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Full text of "Adaptive functions of fleshy ornamentation in wild turkeys and related birds"

ADAPTIVE FUNCTIONS OF FLESHY ORNAMENTATION IN 
WILD TURKEYS AND RELATED BIRDS 



By 
RICHARD BUCHHOLZ 



A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL 

OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT 

OF THE REQUIREMENTS FOR THE DEGREE OF 

DOCTOR OF PHILOSOPHY 



UNIVERSITY OF FLORIDA 
1994 



"That's the whole problem with science. 

You've got a bunch of empiricists 

trying to describe things of unimaginable wonder." 

Calvin 



ACKNOWLEDGEMENTS 

My advisor, Jane Brockmann, has gone above and beyond the call of duty in helping 
me with this project I will always be grateful for her enthusiasm, advice, instruction, 
guidance, constructive criticism and support. Little did I know that an academicumwelt is 
learned as well as innate, just like everything else. 

This study would not have been possible without the help of the rest of my 
committee. Ellis Greiner kindly taught me parasitology and allowed me to use his lab. He 
has also been very tolerant of the strange questions we ask over on this side of Archer Rd. 
Rich Kiltie has thought carefully about the theoretical underpinnings and techniques I have 
used to study fleshy structures. He directed me at several crucial turning points and made 
me realize the consequences of my assumptions (although I suspect he does not find 
turkeys very aesthetically pleasing). Doug Levey has always encouraged and helped me by 
considering even my wackiest ideas with tact He is also my secret source for everything 
"birdy." Brian McNab taught me about physiological ecology and generously allowed me 
to use his lab. Dave McDonald has served as a "ghost" committee member and a friend 
during my entire graduate career. 

Literally dozens of people helped catch, handle and process wild turkeys. I am 
grateful for their help. This study would not have been possible without it. In particular I 
would like to thank those who helped me several times, including Laurie Eberhardt Ron 
Clouse, Paula Cushing, and Monica Marquez. Farol Tomson and Frank Nordlie found a 
place to keep the turkeys, the Department of Zoology paid the costs of maintaining them, 
and Chris Wilcox and her crew helped care for the turkeys when I was out of town. The 
Florida Museum of Natural History, University Athletic Association and Frank Maturo 



in 



generously allowed me to use their facilities to house the turkeys. My dad, Eduard 
Buchholz helped improve the turkey cages. Margaret Byrne and Gerry Ryan helped build 
new cages. 

My studies of free-living wild turkeys were done under permit from the Florida 
Department of Natural Resources and Florida Game and Freshwater Fish Commission. 
Permits were facilitated by Dan Pearson and David Cobb. I thank them and the staffs at 
Paynes Prairie State Preserve and Camp Blanding Wildlife Management Area, particularly 
Jim Weimer and Jack Gillen. The National Wild Turkey Federation provided wild turkey 
transport boxes free of charge. 

Several pilot studies did not pan out in the long run. Nevertheless I would like to 
thank those who assisted me in these preliminary efforts. John Eisenberg kindly provided 
permission to conduct preliminary research at the Katharine Ordway Preserve. Peter and 
Denise Buchholz figured out how to catch jungle fowl on Kauai. Steve Nesbitt taught me 
all about sandhill cranes, shared his data and let me tag along on crane capturing trips. 
Marilyn Spaulding, Don Forrester and Sam Telford helped with my earliest attempts at 
parasitology. I hope they will continue to encourage students as they did me. 

At times graduate school is a very frustrating and unrewarding place. I must thank 
the family and friends who have supported, laughed and commiserated with me over the 
years and made it better. All have been instrumental in keeping me (somewhat) sane and 
(usually) happy. Nothing would have been possible without the love and generosity of my 
parents, Eduard and Elisabeth Buchholz. I hope someday they understand why I had to do 
this. Gratitude goes to their son Peter, who reaffirmed our brotherhood despite having 
chosen a different path. Thanks go to Marianne von Osten and Susan Edelbach, my "aunt" 
and "sister," for always welcoming me home. Special thanks go to fellow cohort member, 
peer advisor and buddy Laurie Eberhardt. I will miss her (boo!) and Peter. Carlita 
Restrepo is a kindred spirit. I thank the expatriates, Tes Toop and John Donald, for being 
funny, stabilizing and never dull. They tell me that in Australia Occam's razor is used to cut 



IV 



Gordian knots. Monica Marquez made sure I finished my NSF grant application and has 
always been an encouraging friend. Margaret Byrne and Gerry Ryan have been kind to me 
in many ways. I value my friendship with each of them and hope they figure out what they 
are looking for. Renee Calarco and Barbara Crute helped me get here, helped keep me here, 
and were always there. Maggie and Ted would not be happy about being mentioned in the 
same sentence, but I cherished them both. John, Tom, Bubba and Jane taught me alot about 
turkeys; may they rest in peace. 

Last, but not least, I thank the office staffs: Carol "Sweet Cheeks" Binello, Alice 
"Glamour Girl" McClaughry, Janet "Green Thumb" Zeigler, Lynda Everitt, Lori "Where 
Are You Going?" Clark, Ruth Ann Czerenda, Evelyn Rockwell, Kenetha "I've Got my Eye 
on You" Johnson, Tangelyn "You're Crazy" Mitchell and, of course, Gracie "Babes" Kiltie. 
Also thanks to Pete in the stockroom. They kept life in Bartram and Carr interesting and 
smoothed over the red tape. Keep up the great job! 

My research was funded by the Department of Zoology at the University of Florida, 
a Frank M. Chapman Memorial Fund Grant in Ornithology from the American Museum of 
Natural History, a grant-in-aid of research from Sigma Xi, the Animal Behavior Fund of the 
University of Florida Foundation, the Cracid Breeding and Conservation Center, and a 
Threadgill Dissertation Fellowship from the College of Liberal Arts and Sciences at the 
University of Florida. 



TABLE OF CONTENTS 

ACKNOWLEDGEMENTS iii 

ABSTRACT viii 

CHAPTERS 

1 GENERAL INTRODUCTION 1 

2 A COMPARATIVE ANALYSIS OF THE ADAPTIVE 

SIGNIFICANCE OF FLESHY STRUCTURES IN THE 

GALLIFORMES 5 

Hypotheses and Predictions 7 

Inter-individual Assessment 7 

Immediate benefits 9 

Good genes models 10 

Fisher's runaway selection 13 

Thermoregulation 13 

Fleshy structures as heat sinks 14 

Solar collector 14 

Methods 15 

Results 18 

Inter-individual Assessment 18 

Immediate benefits 18 

Good genes models 18 

Thermoregulation 22 

Fleshy structures as heat sinks 22 

Solar collector 22 

Discussion 22 

3 ADAPTIVE FEMALE CHOICE FOR MALE FLESHY 

ORNAMENTATION IN WILD TURKEYS 25 

Introduction 25 

Methods 30 

Study Species 30 

Mate Choice Experiments 31 

Live male experiment 32 

Male model experiment 37 

Correlates of Ornamentation in Wild Males 39 

Results 40 

Live Males Experiment 40 

Male Models Experiment 42 

vi 



Correlates of Ornamentation in Wild Males 43 

Discussion 46 

4 MALE DOMINANCE AND VARIATION IN FLESHY HEAD 

ORNAMENTATION IN WILD TURKEYS 51 

Introduction 51 

Methods 53 

Live Males 54 

Male Model Trials 56 

Results 57 

Live Male Trials 57 

Male Model Trials 62 

Discussion 62 

5 THE THERMOREGULATORY ROLE OF THE UNFEATHERED 

HEAD AND NECK IN MALE WILD TURKEYS 66 

Introduction 66 

Methods 67 

Subjects and Apparatuses 67 

Experimental Design 69 

Results 71 

Discussion 79 

GENERAL DISCUSSION 82 

LIST OF REFERENCES 85 

BIOGRAPHICAL SKETCH 94 



vn 



Abstract of Dissertation Presented to the Graduate School 
of the University of Florida in Partial Fulfillment of the 
Requirements for the Degree of Doctor of Philosophy 

ADAPTIVE FUNCTIONS OF FLESHY ORNAMENTATION 
IN WILD TURKEYS AND RELATED BIRDS 

By 

Richard Buchholz 

August, 1994 

Chairman: H. Jane Brockmann 
Major Department: Zoology 

Wattles and other types of unfeathered fleshy ornamentation in birds are puzzling to 
evolutionary biologists because these structures increase the bird's susceptibility to blood- 
feeding insects and heat loss, without providing any obvious benefits. This study tests 
sexual and nonsexual hypotheses for the evolution and maintenance of fleshy 
ornamentation in galliform birds, particularly the wild turkey (Meleagris gallopavo) . 

A comparative study of the elaboration of fleshy structures in the avian order 
Galliformes identified the evolutionary pressures under which fleshy structures may have 
evolved. After controlling for the effects of body size and shared phylogeny, the lack of 
clear cut associations between fleshy ornamentation and other types of ornaments suggests 
that sexual selection has not played an important role in the evolution of these structures. 
Strong negative correlations with latitude, on the other hand, are supportive of a 
thermoregulatory role for these characters. 

Sexual selection for the maintenance of fleshy ornamentation was tested in mate 
choice and dominance trials using wild turkeys raised in captivity. If the wild turkey's 

viii 



fleshy structures are maintained by female choice, females are expected to mate non- 
randomly with respect to these characters. Females chose males with greater snood lengths 
and skullcap widths. Males with longer snoods were more likely to be dominant in dyadic 
encounters. In complementary field studies in north central Florida, male snood length was 
found to be a "good genes" indicator of coccidia infection and body condition. Thus the 
turkey's snood appears to be maintained by female choice for males who signal their genetic 
quality. 

The extensive vascularization of fleshy ornamentation suggests that it may function 
in thermoregulation. By insulating the unfeathered bare heads and necks of wild turkeys, I 
tested whether the fleshy ornamentation of this species is important in heat dissipation. 
Insulated turkeys increased their oxygen consumption and experienced higher body 
temperatures relative to uninsulated controls. These results concur with those of the 
comparative study and suggest avian fleshy structures function in heat dissipation as well as 
sexual selection. Nonsexual hypotheses for the maintenance of ornamentation in animals 
are rarely proposed, but are necessary to understand the evolution of these costly characters. 



IX 



CHAPTER 1 
GENERAL INTRODUCTION 



Brightly colored plumage, large branching antlers and delicately curved horns, 
elaborate tails and courtship behaviors in animals seem inconsistent with our general notion 
of the parsimony of nature. These characters are often called "extravangant" or 
"ornamental" because they are particularly striking in appearance to human observers and 
detailed studies of their function have not been conducted. They are ornamental in the sense 
that they make the bearer physically more obvious without having any direct, functional 
purpose, such as in catching food items or digging burrows. These extravagant characters 
may increase the predation risks of animals that have them and likely have costs in terms of 
the energy needed to grow and maintain them. Despite the potentially high costs of having 
extravagant ornamentation, little is known of the benefits. However the dramatic physical 
appearance of these structures, coupled with their development at reproductive maturity or 
seasonally with breeding has led most authors to suggest that they have evolved via sexual 
selection, that is that they have some function in increasing mating success. Thus the high 
costs associated with ornamentation are assumed to be counterbalanced by increased 
reproductive success. Assumptions about the adaptive benefit of "ornamental" structures 
under sexual selection often make intuitive sense. Unfortunately additional hypotheses that 
might explain how these traits evolved over time or how they are currently maintained are 
rarely considered. The goal of my doctoral research is to propose and test both sexual and 
nonsexual hypotheses for the evolution and maintenance of a subset of avian ornamentation 
commonly called fleshy structures (FS). 



Combs, ceres, wattles and similar fleshy structures are widespread in the class Aves, 
but are particularly common in the order Galliformes (quails, pheasants, grouse, curassows, 
guans, megapodes). Despite the frequency of these fleshy characters, there has never been a 
thorough examination of their adaptive significance. First, I conduct a comparative analysis 
of the morphological and ecological correlates of FS in the Galliformes to test four 
alternative hypotheses for the evolution of these anomalous structures (Chapter 2). These 
hypotheses fall into two functional groups that are not necessarily mutually exclusive: (1) 
inter-individual assessment and (2) thermoregulation. After examining the interspecific 
correlates of fleshy ornamentation in this avian order, I evaluate these hypotheses in a local 
galliform, the wild turkey (Meleagris gallopavo) . in subsequent chapters. 

Male wild turkeys are perhaps the most ornamented birds in North America. They 
have iridescent feathers, a hair-like beard projecting from their chest and most notably an 
unfeathered, bright red, white and blue head and neck. On the head and neck are three types 
of extravagant fleshy projections. Perhaps the most remarkable is the distensible frontal 
process or snood hanging over the bird's bill. At the base of the neck are large fleshy 
protuberances called frontal caruncles and on the side of the neck are small polyp-like 
fleshy structures called side caruncles. During display these fleshy structures change 
markedly; the snood distends and the caruncles are flushed with blood and become bright 
red. The association of this change with courtship suggests that these fleshy structures 
affect mating success. 

Sexual selection is divided into two subsets: female choice and male-male 
competition for access to females. If female choice is an important selective factor 
maintaining male fleshy ornamentation in wild turkeys, variability in male ornamentation 
should affect male mating success (Chapter 3). Similarly if male-male competition is a 
significant selective pressure, variability in fleshy ornamentation should affect the outcome 
of male-male interactions (Chapter 4). Two general models of female choice for male 
fleshy structures are tested: "good genes" and "arbitrary preferences." Both types predict 



that females will exert directional selection for the more exaggerated form of male 
ornamentation. Good genes models propose that the character in question is assessed by 
females because it is an indicator of the heritable vigor of the bearer, but the arbitrary 
preference model predicts no such association between ornament and male viability. To 
investigate how wild turkey ornamentation may have evolved by female choice, the 
assumptions and predictions of these models must be tested. First, do females mate 
randomly with respect to male traits, and if not, which traits do they assess in prospective 
mates? Second, are the characters assessed by females particularly good indicators of the 
male's success in dealing with factors limiting the fitness of wild turkeys? One factor 
limiting fitness of males is their ability to displace other males away from females during 
the reproductive season. 

Wild turkeys are a highly polygynous species in which males attempt to restrict the 
access of other males to groups of females during the mating season. Thus agonistic 
interactions and social dominance may be important determinants of reproductive success. 
Females may prefer to mate with dominant males if components of dominance are heritable 
and will be passed on to their offspring. Subordinate males should avoid dangerous battles 
with dominant males if they have tittle chance of winning. Fleshy ornamentation may play a 
role in mutual assessment before male battles, because these structures appear to be good 
indicators of condition and testosterone levels in related galliform species. To see if this is 
the case in wild turkeys, the value of fleshy ornamentation in indicating the outcome of 
male-male combat is assessed. Then I ask whether males actually judge the ornamentation 
of other males before interacting with them. 

Female choice and male-male competition are not the only hypotheses that might 
explain the maintenance of fleshy ornamentation in wild turkeys. Fleshy ornamentation is 
highly vascularized and may be used in thermal balance, particularly at high temperatures. 
The value of unfeathered ornamentation in dissipating heat at high temperatures and the cost 



of an uninsulated head and neck at low temperatures is assessed by experimentally 
reinsulating the heads and necks of wild turkeys as though they were feathered (Chapter 5). 

Ornamental structures and elaborate courtship behavior patterns in animals have 
long puzzled evolutionary biologists. Recent work on these characters, which are often 
quite bizarre in appearance, suggests that these evolutionary puzzles are not always 
attributable to sexual selection. Natural selection can mold the specific characteristics of 
sexually selected characters to minimize their costs, and it can select for structures that share 
characteristics with sexually selected traits, but that have very practical functions outside of 
mate choice and male-male competition. The goal of this study is to understand the 
evolution and maintenance of fleshy ornamentation in galliform birds. 



CHAPTER 2 
A COMPARATIVE ANALYSIS OF THE ADAPTTVE SIGNIFICANCE OF "FLESHY" 

STRUCTURES IN THE GALLIFORMES 



Introduction 

Combs, ceres, wattles, knobs, snoods and other fleshy structures are a virtually 
unstudied evolutionary puzzle in avian biology. These areas of bare skin, often called 
"fleshy" structures, are present in some members of at least 30% of bird families. In some 
small families, fleshy structures are found in every species (e.g., Casuariidae, Fregatidae, 
Callaeidae); in other larger families, fleshy structures are nearly fixed (e.g., Gruidae and 
Cracidae) or widespread (e.g., Phasianidae and Meliphagidae). Fleshy structures appear to 
be completely absent in only 1 1 of the 27 avian orders (Table 2-1). Oddly, despite the 
frequency of these fleshy characters and their importance to avian taxonomy, there has never 
been a thorough examination of their adaptive significance. 

FS are generally assumed to be sexual ornamentation (e.g., Welty 1975) and recent 
empirical studies provide strong support for both intersexual and intrasexual explanations 
for the maintenance of these structures (Brodsky 1988; Boyce 1990; Hillgarth 1990; Ligon 
et al. 1990; Zuk et al. 1990a; 1990b; 1992; Holder & Montgomerie 1993). Unfortunately 
none of these investigations has addressed nonsexual functions for these structures. In 
addition no studies have addressed the costs inherent to having exposed skin. FS are a 
chink in the protective armor (feathers and scales) covering a bird's body surface. Exposing 
bare skin to a world of temperature extremes, aggressive competitors and disease-carrying 
insects would seem to be maladaptive. Have birds evolved these seemingly costly characters 
solely in the context of increased mating success? 



Table 2-1. Fleshy structures are found in 47 families in 1 1 orders in the Class Aves. 



• Struthioniformes 

Struthionidae* 
A Rheiformes 
Rheidae 

• Casuariiformes 
Casuariidae* 
Dromaiidae* 

A Apterygiformies 

Apterygidae 

A Tinamiformes 

Tinamidae 

A Sphenisciformes 

Spheniscidae 

A Gaviiformes 

Gaviidae 

A Podicipediformes 

Podicipedidae 

A Procellariiformes 

Diomedidae 

Procellaridae 

Hydrobatidae 

Pelecanoididae 

• Pelecaniforrnes 
Phaethontidae 
Pelecanidae* 
Sulidae 

Phalacrocoracidae* 
Anhingidae 
Fregatidae* 

• Ciconiiformes 
Ardeidae 
Balaenicipitidae 
Scopidae 
Ciconiidae* 
Threskiornitbidae* 
Phoenicopteridae* 

• Anseriformes 
Anhimidae 
Anatidae* 

• Falconifo nines 
Cathartidae* 
Pandionidae 
Accipitridae* 
Sagittaridae* 
Falconidae 

• Galliformes 
Megapodiidae* 
Cracidae* 
Pbasianidae* 
Opisthocomidae* 



• Gruiformes 

Mesitomithidae 

Tumicidae 

Pedionomidae 

Gruidae* 

Aramidae 

Psophiidae 

Rallidae 

Heliornithidae 

Rhynocetidae 

Eurypygidae 

Canamidae* 

Otididae* 

• Charadriiformes 
Jacanidae* 
Rostratulidae 
Dromadidae 
HaematDpodidae 
Ibidorhychidae 
Recurvirorostidae 
Burbinidae 
GlareoUdae 
Charadriidae 
Scolopacidae* 
Thinocoridae 
Chionididae* 
Stercorariidae 
Laridae 
Rynchopidae 
Alcidae* 

• Columbiformes 
PterocUdidae 
Columbidae* 

• Psittaciformes 
Psittacidae* 
Loriidae* 
Cacatuidae* 

• Cuculiformes 
Musophagidae* 
CucuUdae* 

A Strigiformes 

Tytonidae 

Strigidae 

A Caprimulgiformes 

Steatomitbidae 

Podargidae 

Nyctibiidae 

AegotheUdae 

Caprimulgidae 



A Apodiformes 
Apodidae 
Hemiproaiidae 
TrochUidae 

• Coliiformes 
CoUidae* 

A Trogoniformes 
Trogonidae 

• Coraciiformes 
Alcedinidae 
Todidae 
Momotidae 
Meropidae 
Coraciidae 
Brachypteraciidae 
Leptosomatidae 
Upupidae 
Phoeniculidae 
Bucerotidae* 

• Piciformes 
Galbulidae 
Bucconidae 
Capitonidae* 
Indicatoridae 
Ramphastidae* 
Picidae* 

• Passeriformes 
Eurylaimidae 
Dendrocolaptidae 
Fumariidae 
Formicariidae* 
Conopophagidae 
Rhinocryptidae 
Cotingidae* 
Pipridae 
Tyrannidae 
bxyruncidae 
Phytotomidae* 
Pittidae 
Xenicidae 
Philepittidae* 
Menuridae 
Atrichoraithidae 
Alaudidae 
Hinmdinidae 
Motacillidae 
Campephagidae 
Pycnonotidae 
Irenidae 



Laniidae 

Vangidae 

BombyciUidae 

Dubdae 

Cindidae 

Troglodytidae 

Mimidae 

PruneUidae 

Muscicapidae* 

AegathaUdae 

Remizidae 

Paridae 

Sittidae 

Certiidae 

Rhabdornithae 

CUmacteridae 

Dicaeidae 

Nectariniidae 

Zosteropidae* 

Melapbagidae* 

Emberizidae 

Parulidae 

Drepanididae 

Virecaiidae 

Icteridae* 

Fringillidae 

Estrildidae 

Ploceidae 

Sturnidae* 

Oriolidae* 

Dicnjridae 

Callaeidae 

Grallinidae 

Aratamidae 

Cracticidae 

Ptilonorhynchidae 

Paradisaeidae 

Corvidae 



Classification follows Morony et al. (1975). Field guides were examined to identify taxa with FS. 
All species were not examined, tbus additional taxa may possess FS. Famines without annotation 
lack fleshy structures; • order contains at least one species with a fleshy structure; A no fleshy 
structures present in representative species surveyed in each family of order; * family contains at 
least one species that possesses a fleshy structure. 



Although it is ordinarily not possible to know the selective pressures under which any 
trait evolved in the past, comparative analyses of the environmental, morphological and 
ecological correlates of traits across species provide clues to the selective factors associated 
with their evolution (Clutton-Brock & Harvey 1984). I conducted such an analysis to test 
four alternative hypotheses for the evolution of FS in the Galliformes (quails, pheasants, 
grouse, curassows, guans, megapodes). Galliformes are well suited for such a study 
because their behavior, ecology and distributions are fairly well documented. They exhibit a 
diversity of FS that are familiar to anyone who has seen a domestic chicken or turkey. 

FS are not fleshy, that is, they contain very little muscle tissue. As used in common 
parlance, however, "fleshy" accurately describes the soft or pliable nature of FS. Fleshy 
structures (FS) vary greatly among taxa in size, shape, color and location and in their use 
during display (Figure 2-1). Depending on the species, intraspecific variation in the color, 
shape or presence of FS can be associated with sexual maturity (Hollett et al. 1984), 
seasonal changes (Stokkan 1979), age (Buchholz 1991) and changes in motivation 
(Johnsgard 1983; Franklin & Menkhorst 1988; Reichholf 1988). Consistent with the 
extensive variation in the external morphology of FS is a wide range of hypotheses in the 
literature on the adaptive functions of exposed skin in birds. These hypotheses generally 
fall into two major, functional groups that are not necessarily mutually exclusive: (1) inter- 
individual assessment and (2) thermoregulation. In the next section, I describe these 
hypotheses and develop predictions for testing and distinguishing among them. 

Hypotheses and Predictions 

Inter-individual Assessment 

The apparent association of FS with sexual maturity suggests that they are an important 
form of sexual ornamentation. Several hypotheses suggest that sexual ornamentation 
functions in inter-individual assessment (i.e. an individual evaluates the ornaments of 




Figure 2- 1 . Diversity of fleshy structure size, shape and change during display in the 
Galliformes. Unfeathered areas (FS) bordered by stippling, a) and b) bare orbit and eye 
wattle of male Syrmaticus pheasant before and during display, respectively; c) bare orbit 
and dewlap of Pipile guan; d) bare head, neck and collar wattle of brush turkey, Alectura : e) 
bare orbit of male wood partridge, Rollulus : f) knob, cere and wattles of a male curassow, 
Crax : g) eye combs of male black grouse, Tetrao , during display; h) and i) cere and cere, 
horns and throat lappet in male Tragopan before and during display, respectively. 



another individual and this information determines whether or how they interact). 
Traditionally, sexual selection theory has been divided into two subdisciplines: female 
choice and male-male competition. FS, then, may be used for assessment both by females 
and by other males. Females may assess a male's parental ability, his ability to provide 
access to resources, his genetically based viability, or other features (Johnson & Mazluff 
1990). Similarly, males may use the same or different characters to assess other males 
prior to aggressive interactions (Borgia 1979; McKinney et al. 1990), or rarely, females. A 
true test of these hypotheses requires standardized studies of the mate choice and 
competitive behavior of each species. Instead I have assumed that if FS are subject to 
assessment, they will co-occur with other characters that have been shown to be subject to 
assessment in other species. All inter-individual assessment hypotheses assume that 
females prefer males with the most exaggerated FS and that males will not fight as readily 
with such males. 
Immediate benefits 

A male's epigamic traits may reveal direct benefits to the female such as his ability to 
provide parental care, to feed the female during courtship, or his dominance over good 
foraging areas. Female choice on these characters is favored because she and her offspring 
benefit directly, rather than receiving indirect benefits from increased survivorship under the 
good genes models discussed below (Kirkpatrick 1987). Jf FS have evolved to signal a 
male's ability to provide immediate benefits, then the following predictions can be made. 

(i) Fleshy structures will be most common and largest in breeding systems where males 
most commonly provide immediate benefits to the female and her young (i.e. in 
monogamy). 

(ii) Because males and females have similar variance in mating success in monogamous 
systems (Payne 1984), making mutual assessment more likely, the sexes can be expected to 
be more similar in FS size than in non-monogamous species. 



10 

Good genes models 

If differences in general viability (e.g., health, dominance) are due to genotypic 
differences, females may be able to choose these "good" genes for their offspring 
(Andersson 1986; Heisler et al. 1987). Female choice for good genes may be especially 
important in systems where the male provides no care or other resources for the female or 
young. In this case traits that honestly advertise male condition will be chosen by females 
(Kodric-Brown & Brown 1984). The following hypotheses address specific viability 
correlates that females may use to assess males (and that other males may avoid in 
combatants). 

Parasite resistance . Hamilton and Zuk (1982) proposed that FS in birds are utilized in 
the assessment of blood parasite burden in prospective mates. Avian blood parasites may 
reduce fecundity (Korpimaki et al. 1993) or survivorship (Atkinson & van Riper 1991; 
Bennett et al. 1993). At some stage in their life cycle, hematozoa lyse the blood or muscle 
cell they occupy and release merozoites (asexual sister cells that subsequendy infect other 
blood cells or tissues) or gametocytes (which are picked up by insect vectors during blood 
feeding). Red blood cell lysis or muscle impairment may result in anemia that is detectable 
in the color or turgidity of highly vascularized FS. 

The Hamilton-Zuk hypothesis can be expanded to include other parasites or parasitic 
mechanisms that may affect the size or color of FS. For example, intestinal coccidia 
infection is associated with reduced blood carotenoid levels (Ruff et al. 1974) and may 
affect FS pigmentation. Ligon et al. (1990) and Zuk et al. (1990b) found that infection with 
the intestinal nematode Ascaridia reduced comb size in male junglefowl and that females 
preferred males with larger combs (above a threshold size), and big combed males were 
more successful in male-male contests. Hillgarth (1990) found a negative correlation 
between coccidia burden and mating success in ringneck pheasants and showed that males 
that extended their face wattles fully and for long periods had higher mating success 
(although she does not mention a direct correlation between wattle size and parasite burden). 



11 

Ectoparasites may also affect ornamentation and mating success. Spurrier (1991) applied 
pigment marks resembling hematomas caused by lice on the cervical air sacs of Sage 
Grouse and found that females preferred the unblemished males. Unfortunately the only 
measures of parasite prevalence available for most galliform species is of the blood 
parasites, therefore I restrict my predictions to this group. 

(i) Species with FS should be more susceptible to parasitic infection than non-FS 
species (Hamilton & Zuk 1982; Read 1987). The unidirectional nature of this prediction 
may seem counter intuitive. However, since female choice for resistant males may result in 
higher mean resistance in the next generation, the co-evolutionary nature of host-parasite 
interactions insures that over long periods of evolutionary time, the host will continue to be 
susceptible to the parasite. This is a result of adaptations by the parasite that counter the 
host's new defenses. 

(ii) Fleshy structures should be larger, more sexually dimorphic and show greater 
change during display in species with higher prevalences of hematozoa. 

Plumage brightness . Female preference for brighter or more boldly plumaged males is 
well documented in the avian literature (Burley et al. 1982; Zuk et al. 1992; Johnson et al. 
1993; Hill 1994). Brighter males may have access to more or better quality food, be less 
susceptible to parasites or be more dominant Alternatively females may merely prefer more 
brightly colored males with no naturally selected advantage, sensu Fisher (Fisher 1958). In 
any case, if females are choosing males based on their ornamentation, an association 
between plumage brightness and FS presence and size might be expected. 

(i) Species with FS should have brighter plumage than those lacking FS. Also FS size 
should be larger in brighter species. 

(ii) Species with FS should be more likely to have other types of ornamentation 
associated with reproductive displays, such as crests and elaborated tails. 



12 

(iii) If sexual dimorphism in FS size can be attributed to the same selective pressure as 
sexual dichromatism, namely female choice, then these types of dimorphism should be 
positively correlated with one another. 

Dominance interactions . If social dominance provides access to resources, females that 
choose dominant males may give their offspring a genetic advantage (as well as direct 
benefits in systems with paternal care or territoriality). If male-male competition selects for 
the advertisement of male quality via FS ornamentation (Borgia 1979), females merely need 
to select the male with the best FS. How might FS signal male dominance? Fleshy 
structure growth seems to be mediated by testosterone (references in Ligon et al. 1990). 
Testosterone has been linked with aggression in many animals and is related to dominance 
in some birds (Wingfield et al. 1987). Therefore dominant males with high testosterone 
levels may have the biggest FS. For example, in ptarmigans (Lagopus spp.) male comb size 
is correlated with dominance (Moss et al. 1979), testosterone injections increase comb size 
(Stokkan 1979), and males with bigger combs have higher mating success (Brodsky 1988). 
Similar correlative relationships between FS size, testosterone and dominance status are 
found in red jungle fowl (Gallus gallus : references in Ligon et al. 1990). Presumably, 
intrasexual selection is a precondition for female choice for male dominance. If FS have 
evolved for intrasexual signalling the following predictions can be made. 

(i) Across species FS should be associated with systems in which male-male 
competition is most acute (i.e. in polygyny). 

(ii) Fleshy structures should be positively associated with characteristics important to 
male-male competition, such as sexual size dimorphism (Payne 1984) and the presence and 
sexual dimorphism of weapons such as tarsal spurs (Ligon et al. 1990). 

Other good genes models . The inherent costs of FS in terms of heat loss and insect 
damage would suggest that these structures may serve as handicaps (Zahavi 1975; Grafen 
1990a; 1990b). Handicapping traits make it more difficult for males to survive and by 
doing so reveal to females the males heritable vigor. Although such traits reduce average 



13 

male survivorship, all the offspring of males who survive despite the handicap inherit their 
fathers' good genes and the sons inherit their fathers' attractive ornament as well. 
Unfortunately the handicap model makes no comparative predictions about FS. 
Fisher's runaway selection 

This process, called arbitrary by some authors (Kodric-Brown 1993), has no 
comparative predictions (Heisler et al. 1987; Buchholz 1992) because the selective agent is 
random female preference, unrelated to naturally selected fitness advantages and could occur 
under many environmental conditions. 

Thermoregulation 

The high vascularity and exposed nature of FS suggests that they may have some 
function in thermoregulation (Lucas & Stettenheim 1972; Crowe & Crowe 1979; Whittow 
1986). Intuitively it seems that FS should increase both the evaporative and non-evaporative 
(radiation, convection, conduction) components of heat loss. In fact, birds lose a large 
amount of body heat from unfeathered or lightly feathered surfaces such as the legs 
(Baudinette et al. 1976) and head (Hill et al. 1980). This heat loss may be detrimental to 
individuals living in environments much colder than their body temperature (Whittow 1986; 
Gray & Price 1988). In species living in hot environments, however, heat loss from the 
head may be essential to general homeostasis. Specific vascular adaptations may facilitate 
heat loss to protect heat sensitive tissues. For example, a counter current heat exchange 
system around the eye, the rete mirable opthalmica , is thought to keep the brain cooler 
than the deep body temperature in some birds (Whittow 1986). Alternatively, 
vascularization near the exterior of the animal may aid in the collection of solar heat when 
the surrounding air temperature is low (Henneman 1988). Thus FS could function in 
thermoregulation in two ways: (a) heat dissipation and (b) heat absorbtion. 



14 

Fleshy structures as heat sinks 

Crowe's (Crowe 1979; Crowe & Withers 1979b; Withers et al. 1980) studies of 
behavior and FS variation in the helmeted guineafowl (Numida meleagris) show that wattle 
size in this species is positively correlated with maximum daily temperature across its broad 
geographic range. Biotelemetric measurements of the brain temperature of captive subjects 
show that these birds maximally exposed FS in warm ambient temperatures and reduced 
total thermal conductance by retracting them in cold temperatures. If FS have evolved for 
this purpose, these predictions follow. 

(i) Fleshy structures should be more likely to occur and FS size should be larger in 
species living at lower altitudes and latitudes. As species ranges get further from the 
equator they have less need for dissipating heat 

(ii) Similarly sexual dimorphism in FS size should be reduced in species living at lower 
altitudes and latitudes. As species ranges approach the equator, it becomes equally 
important for both sexes to lose excess body heat. 

(iii) Change in FS size during display should be more pronounced nearer the equator if 
these structures are used to dissipate the excess body heat generated by energetically active 
display. 
Solar collector 

To maintain body temperature during cool conditions, FS may be used to absorb heat 
from the environment instead of increasing metabolic activity (Burtt 1986). The predictions 
of this hypothesis are the reverse of those for the Heat Sink hypothesis above. 

(i) Fleshy structure occurrence and size should be positively correlated with upper 
latitudinal and altitudinal limits of species. 

(ii) Because it should be equally important for both sexes to collect radiation in colder 
areas, sexual dimorphism in FS should be negatively correlated with altitude and latitude 

(iii) Because intraspecific studies show that FS size changes only during sexual 
displays and not outside of this context, it is unlikely that size change is important to 



15 

collecting solar radiation. Therefore there should be no relationship between FS size 
change and latitude or altitude. 

Methods 

Despite the extreme variation in shape and usage of FS, they share certain attributes and 
can be divided into three broad categories: (1) sparsely feathered thin skin without 
distinctive coloring (e.g., the lores of hawks); (2) thickened bare skin with or without 
distinctive coloring (e.g., the orbital ring in some parrots); and (3) projections of thickened, 
brightly colored skin (e.g., a chicken's comb). Lumping these three types of structures 
under a single heading may be somewhat unnatural, since bird species may have very 
different reasons for exposing their skin. However, so little is known about the 
morphology, associations and functions of these variable structures that I think this 
phenomenon warrants an initial investigation at a broader level. Therefore, to identify 
patterns in the function of exposed skin, I initially lump these structures. 

Using literature accounts I collected information on the presence, size, sexual 
dimorphism and size change during display of FS, and on the upper, lower, and mid 
altitudinal and latitudinal limits, body size and sexual dimorphism, mating system, presence 
of spurs, blood parasite prevalence, and plumage showiness (or "brightness," sensu 
Hamilton & Zuk 1982) and sexual dichromatism of 279 species of Galliformes in three 
families (Cracidae, Megapodiidae, Phasianidae). Fleshy structures and plumage 
characteristics were determined from plates and photos in monographs (Delacour & 
Amadon 1973; Johnsgard 1983; 1986; 1988), a variety of field guides, individual accounts 
and personal observations. The FS size of resting males was ranked on a scale of 0-5 
relative to head size. The ranking of FS size relative to head size in all species prevents any 
bias in the results where the FS in question may have been used to establish the underlying 
taxonomy. Sexual dimorphism in FS size was ranked on a scale of 0-2. Fleshy structure 
size change during display was ranked on a scale of 0-5. Plumage brightness was ranked 



16 

on a scale of 0-5. Sexual size dimorphism was calculated as the average male mass divided 
by the average female mass. Mating system was ranked on a scale of 1-3 based on the 
degree of polygyny thought to commonly occur in each species. The average number of 
spurs on males of each species (Davison 1985) was included in the analysis as a measure of 
male-male competition. Sexual dimorphism in spur number was measured as the female 
value subtracted from the male value. Maximum and minimum altitudinal limits were 
collected from species accounts and latitudinal limits were estimated from range maps. 
Blood parasite prevalences (proportion of sampled individuals found to be infected) were 
collected from regional surveys or reviews (Oosthuizen & Markus 1967; 1969; Greiner et 
al. 1975, Ashford et al. 1976; Bennett & Herman 1976; Wink & Bennett 1976; McClure et 
al. 1978; White et al. 1978; Peirce 1981). 

Recently a number of new cladistic methods that control for the nonindependence of 
data points due to shared phylogeny have been developed for comparative studies (Harvey 
& Pagel 1991). Many of these assume a "true" phylogeny of the organisms under study. 
Unfortunately the phylogeny of the Galliformes does not meet this condition because it is 
in constant flux (Randi et al. 1991) and has had very few molecular studies at lower branch 
points. The comparative technique I used controls for the effects of shared phylogeny by 
averaging measurements within nested taxonomic subsets (i.e. averaging the species within 
each genus, then genera within tribes) and examining the correlations of these averages at 
each of these taxonomic levels. Pagel and Harvey (1988) have suggested conducting 
statistical analyses of these data at the single taxonomic level that subsumes the most 
variance. In the gaUiform data set analyzed here, most of the variance in FS characteristics 
is found at the tribe or family level. The decision rule proposed by Pagel and Harvey has 
drawbacks when comparative associations are studied within one avian order because 
sample sizes are considerably reduced at higher taxonomic levels. Statistics cannot be 
employed with only three values at the family level and low sample sizes at the tribe level 
carry with them a high risk of type II error; the inability to detect significant relationships 



17 

between variables when they exist. Therefore, I adopt a more exploratory approach and 
present the associations found between variables at all three taxonomic levels considered: 
species, genus and tribe. Correlational relationships found only at all lower taxonomic 
levels (e.g., across species) may be artifacts of shared phylogeny rather than the products of 
unique evolutionary events. Correlations at higher levels may not be significant because of 
small sample size. However those correlations that retain statistical significance across all 
taxonomic levels probably represent strong adaptive relationships. 

The hypotheses presented for the evolution of FS were tested statistically in three ways. 
First I compared taxa with FS to those lacking these structures. The occurrence of FS was 
tested in a contingency table constructed from the number of taxa above and below the 
median of the pertinent independent variable and the presence or absence of FS. Second the 
factors associated with the elaboration of FS in species that had them were also tested in a 
contingency table. Fleshy structure size and the independent variables were divided into two 
groups at the median. Third the strength of association between three FS characteristics 
(FS size, dimorphism and display change) and the independent variables were tested with 
non-parametric correlation analysis (Spearman rank correlation). Sample sizes vary with 
the availability of data for each variable. The data set lacked complete information for most 
of the megapodes, and therefore these species are poorly represented by the results. 

At the species level, FS size was strongly correlated with body mass. To remove 
correlations between variables caused by their shared correlation with mass, residual values 
generated by regressing each variable with body mass were used in all the analyses. This 
approach assumes that the effect of natural or sexual selection on FS characteristics is direct 
and not mediated by body size. It was not possible to test predictions relating to sexual size 
dimorphism because this variable is calculated from a ratio with male mass as the 
denominator. In the contingeny analyses of the occurrence of FS this resulted in about half 
of the FS with a rank of one being included in the "FS absent" row. Finally, latitude and 
altitude were positively correlated with one another and showed similar associations in most 



18 

tests, so for the sake of brevity results given only for latitude. Except where noted latitude 
refers to the mid-point of the species' range. 

Results 
Inter-individual Assessment 

Immediate benefits 

FS were more common and more elaborate in non-monogamous mating systems. 
However after the effects of body size were removed, there was no difference in the 
occurrence or size of FS between monogamous and non-monogamous taxa (Table 2-2 and 
2-3). Sexual dimorphism in FS size was significandy reduced in monogamous species. 
Good genes models 

Fleshy structures were not more common or larger in more showy species. However, 
sexual dimorphism in FS size was positively correlated with sexual dichromatism (Table 2- 
3). Species with elaborate tails were more likely to have FS at the tribe level. Fleshy 
structures were not significandy more common in polygynously mating species, nor did FS 
size increase with number of spurs or the degree of spur dimorphism. Although sexual 
dimorphism in FS size at the species level was significandy greater in species with above 
median spur dimorphism, this relationship did not persist at higher taxonomic levels. The 
occurrence and elaboration of FS was positively correlated with sexual size dimorphism, but 
this relationship is probably due the fact that more dimorphic species are also larger species. 



19 

Table 2-2. Occurrence of FS in galliforms relative to predictions of hypotheses for 
the evolution of these structures. 

Hypotheses and Species Level Genus Level Tribe Level 

Predictions X 2 (N) . X 2 (N) U (N) 

Tmm^iate Benefits 33+ (204) 0.0 _ (43) -2.3* (8) 

FS more common in 

monogamy 

Pa rasite Resistance q.3 (52) 3.1+ (20) "°- 9 ( 8 ) 

FS more common in 
taxa with high 
prevalence 

Plvftnaffft Brightness 2.4 (204) 3.2+ (43) °'° ^ 

FS more common in 
brightly colored taxa 

FS more common in 2.O (204) 0.0 (43) ~ 2 ' 3 * ^ 

taxa with elaborate 

tails 

FS more common in q.O (202) 2.3 (42) "°* 3 ^ 

taxa with elaborate 

crests 

Dominance 

Interactions 

FS more common in 3 3& + (204) 0.0 (43) ~ 2 -3 a ^ 

polygyny 

FS more common in 2 8 a+ (204) 0- 1 ( 48 ) ~ 1,2 ® 

spurred taxa 

FS more common in 3 ( 43) -0.3 (8) 

taxa sexually D -° ^ VH) 

dimorphic for spurs 

HsaLSink . 6.4* (48) -2-3* (8) 

FS more common rn **./ \iyv> 

taxa with lower 

minimum latitudal 

limits 

-7 1 nQtt 6.8** (48) -1.7 + (9) 

Snlar Collector 2A ( 1% ) 

FS more common in 
taxa with higher 
maximum latitudal 
limits 

+ 09>P>0.05; * 0.05>P>0.01; ** 0.01>P>0.001; a significant, but in opposite 
direction; nearly significant, but in opposite direction. Probabilities are for two-tailed tests. 



20 



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22 
Thermoregulation 

Fleshy structures as heat sinks. 

Fleshy structure size was negatively correlated with latitude, and sexual dimorphism in 
FS size was positively correlated with latitude; that is, FS got smaller and more sexually 
dimorphic at higher latitudes (Tables 2-3). The degree of change in FS size during display 
was predicted to be greatest nearest the equator; however, the opposite relationship was 
obtained. Display change in FS size increased significantly with latitude. 
Solar collector 

Species with higher latitudinal limits were not more likely to have FS, nor did they have 
smaller and more sexually dimorphic FS (Tables 2-2 and 2-3). In addition there was a 
positive correlation between maximum latitude and FS size change during display at the 
genus level. As the minimum latitudinal limits of a species increases, females become less 
likely to have FS and males become more likely to reveal the full extent of their FS size 
only during display. 

Discussion 

Despite the many intraspecific studies demonstrating the importance of FS to inter- 
individual assessment, a comparative analysis did not find much support for this hypothesis 
as an explanation for the evolution of FS across galliform species. This result must be 
interpreted with caution because the expected correlates of inter-individual assessment 
processes (e.g., plumage brightness or spur number) are themselves only hypothesized 
correlates of female choice and male-male competition based on intraspecific studies. A 
true test of this hypothesis would necessitate standardized studies of the mate choice and 
competitive behavior of each species. Instead I have assumed that if FS are subject to 
assessment, they will co-occur with other characters that have been shown to be subject to 
assessment in other species. The veracity of this assumption may depend on what is being 
assessed (Sullivan 1994). Additionally it was not possible to include other characters that 



23 

may be correlated with female choice, such as intestinal parasite prevalences. Even though 
FS size was not correlated with the other measures of ornamentation, sexual dimorphism in 
FS size was positively correlated with plumage dimorphism. This finding suggests that the 
factors controlling these variables are the same. Because plumage dimorphism is generally 
attributed to female choice for male brightness, sexual dimorphism in FS size may also be 
explained by this selective pressure. 

FS characteristics were strongly associated with the latitudinal distributions of species, 
even after controlling for body mass. Fleshy structures were more common, larger and 
more similar between the sexes in species nearer the equator. These results are consistent 
with a heat dissipation function for FS, in congruence with intraspecific studies (Crowe 
1979; Crowe & Withers 1979; Withers & Crowe 1980). Alternatively the inverse 
correlation between size and latitude might be the result of the increased thermoregulatory 
costs of having bare skin in colder regions. The increase in display change at higher 
latitudes is also consistent with a cold-limiting rather than a heat-dissipation explanation. 
However if cold temperatures limit FS size across species, one might expect that FS 
occurrence and elaboration would be most strongly correlated with the maximum latitudinal 
limit rather than the minimum limit This is not the case, suggesting that FS actively 
function in dissipating metabolic heat in species living in warm climates. 

Studies of sexual selection often neglect to propose and test nonsexual hypotheses for 
the maintenance of ornamentation in birds and other taxa. Balmford et al. (1993) have 
suggested that an ignorance of aerodynamics has led evolutionary biologists to attribute 
incorrectly all long bird tails to evolution by sexual selection. They argue that some types 
of long tails are not burdensome nor aerodynamically costly and thus would not make good 
indicators of male condition. Similarly characters that were assumed to be maintained 
solely for social signalling, such as the bushy tails of ground squirrels (Bennett et al. 1984) 
or the ultrasound emissions of some rodents (Thiessen 1979), or for quite mundane 
purposes like feeding, such as the flattened bill of most ducks (Hagan & Heath 1980), may 



24 

also be maintained as a result of their thermoregulatory functions. Considering alternative 
or congruent hypotheses for the maintenance of ornamental characters provides a better 
understanding of how seemingly extravagant characters can be quite functional in a practical 
sense. Unfortunately in the absence of an accurate, detailed phylogeny it is impossible to 
determine if FS first evolved for heat dissipation or in sexual selection. Comparative studies 
of the probable ancestral states of ornamentation and behavior have provided unique insight 
into how sexually selected characters first come under assessment by females (Basolo 
1990; Hill 1994). Similar studies of ornamental characters with both sexually selected and 
naturally selected hypotheses in mind may provide a better understanding of how 
extravagant characters can evolve despite their apparent costs. 

Fleshy structures differ from other forms of ornamentation in many ways. They are 
living integumentary outgrowths and thus have inherent costs that other nonliving forms of 
ornamentation, such as big tails or long spurs, do not possess. Similarly the highly 
vascularized nature of FS makes them more likely to be functional outside of the realm of 
reproduction. Therefore, they are uniquely suited for identifying the conflicting forces of 
sexual and natural selection that produce different suites of elaboration in separate 
populations of the same or closely related species (Endler 1983; Kodric-Brown 1990). A 
recognition among empiricists and theoreticians that ornamental structures may have 
multiple beneficial functions, such as the apparent heat dissipation value of FS, the 
thermoregulatory values of squirrel tails, ultrasonic emissions and duck bills, may advance 
our understanding of the evolution of extravagant characters. 



CHAPTER 3 

ADAPTIVE FEMALE CHOICE FOR 

MALE FLESHY STRUCTURES IN WILD TURKEYS 



Introduction 

The wild turkey (Meleagris gallopavo) is a familiar example of a sexually dimorphic 
species exhibiting an array of extravagant behavioral and morphological characters that 
serve no obvious useful function other than to attract mates. Males weigh more than twice 
as much as females and have iridescent feathers, a large fan-like tail, a long hair-like beard 
projecting from their chest, tarsal spurs and an unfeathered head and neck. The unfeathered 
neck is covered with pebble-like red bumps called side caruncles, that may fuse to form 
horizontal bands of bumpy skin (Figure 3-1). At the base of the front of the neck are three 
or four roughly elliptical pillow-like outgrowths called frontal caruncles. The skullcap on 
the crown of the head has thickened skin that ranges in color from red to white and light 
blue and appears to change depending on the motivational state of the animal. Perhaps most 
striking is a distensible process at the base of the upper bill called the snood. Finally a thin 
dewlap stretches from beneath the lower mandible down to the frontal caruncles. This 
extravagantly ornamented bird is uniquely suited to testing models of female choice because 
it is a highly polygynous species and males associate with females only for mating and 
never provide care for their offspring. 

Although we cannot be sure by which selective process any one of the turkey's 
many ornaments has evolved during the history of this species, the evolutionary history of a 
character can be inferred by examining the selective pressures maintaining such characters 
in the present By testing the mating preferences of captive female wild turkeys and 



25 



26 




Figure 3-1. Unfeathered head ornamentation of mature male wild turkey: a) skullcap; b) 
relaxed snood; c) dewlap; d) frontal caruncles; e) side caruncles. 



27 

examining the correlates of the preferred types of ornamentation in wild males, I investigate 
how female choice may be maintaining the extravagant ornamentation of male wild turkeys. 

Hypotheses of indirect benefits of female choice fall into two types: good genes and 
arbitrary preferences. Both types predict that females will exert directional selection for the 
more exaggerated form of male ornamentation (i.e. they prefer bigger, brighter, louder, etc. 
forms of the trait). Good genes models propose that the character in question is assessed 
by females because it is an indicator of the heritable vigor of the bearer. Male vigor or 
viability is a measure of a male's ability to survive acute or chronic factors that limit fitness. 
There are two principal types of good genes hypotheses. The handicap model (Grafen 
1990a; Zahavi 1975) proposes that ornamentation reduces average male survival enabling 
females to assess any individual male's ability to survive despite his burdensome ornament. 
In this case females that choose to mate with more highly ornamented males have higher 
fitness because of the increased survivorship of their female offspring, who carry the male's 
superior survival genes but do not express the sex-limited genes for handicapping 
ornamentation. Male offspring who have genes for the attractive handicap experience 
increased mating success in addition to increased survivorship. In the other type of good 
genes models, females are assessing male ornamentation because it specifically indicates a 
second, less visible trait determining male fitness. Hamilton and Zuk (1982) propose that 
females assess the quality of male ornamentation because these characters are particularly 
good indicators of the parasite burden of the bearer. In the parasite-assessment model, 
females benefit from choosing the more ornamented males because their offspring will 
inherit the male's ability to avoid deleterious infection. In similar models, the male's 
foraging success (Kodric-Brown 1989) or age (Manning 1985; 1989) is honestly indicated 
by his ornamentation. 

Arbitrary preference models, on the other hand, hypothesize that the character 
reveals nothing of the abilities or heritable vigor of the male but is nonetheless preferred by 
females. Fisher's (1958) theory of runaway selection proposed that an initial female 



28 

preference for a male character that came about by natural selection or genetic drift could 
become genetically linked to the male trait, resulting in elaboration of the trait beyond its 
original utility. Similarly other authors (Kirkpatrick 1987; Enquist & Arak 1993) suggest 
that specific attributes of male characters, such as color, shape or frequency, elaborate over 
evolutionary time because they more effectively stimulate existing biases in the sensory 
system of the female. In these models male offspring of females exercising an arbitrary 
preference have greater reproductive success due to the character they inherit Because the 
arbitrary preference model is empirically distinguishable only by the absence of a 
correlation between the male character and measures of male viability, it proves difficult to 
test The arbitrary preference model remains a default or null hypothesis in studies where a 
female preference is detected but the adaptive reason for the preference is not explained by 
the good genes model (Buchholz 1991). The only way to distinguish between the good 
genes and arbitrary models of female choice, when it is not possible to monitor the next 
generation, is by examining the relationship between variation in ornamentation and 
variation in male viability. 

Extensive research on the factors limiting population size in wild turkeys suggests 
three major selective pressures: diseases and parasites, predation, and weather (Dickson 
1992). Population surveys have detected over 100 species of viral, bacterial, fungal, 
protozoal, metazoal and arthropod parasites that may limit the fitness of turkeys (Davidson 
& Wentworth 1992). Although the impact of most of these parasites on their hosts is 
unknown, experimental studies using domestic or captive wild turkeys have suggested that a 
poxvirus (Forrester 1991), a proventricular nematode (Hon et al. 1975; 1978), and blood 
parasites (Forrester et al. 1974; 1980; Atkinson et al. 1988) have the most severe impact on 
host survival, particularly of juveniles. High levels of predation on nests and on nesting or 
brooding females is well documented (Miller & Leopold 1992). Finally weather conditions 
in the northern areas of the wild turkey's range affect survivorship and fecundity. 
Populations subject to deep snow can suffer widespread starvation and mortality 



29 

approaching 60% (Healy 1992b). Food limitation during winter is probably not limited to 
the northern areas of the wild turkey's distribution. A twenty-fold increase in visits to 
artificial feeders during Jan-March suggests that winter food may be limited in Florida as 
well (Powell 1965). How might females detect males that are superior in their abilities to 
cope with these factors? 

The handicap model predicts that females will prefer ornaments that reduce male 
survival. These might be characters that make males more subject to predation, invite 
challenge from competitors or increase the risk of starvation. To test the handicap principle 
of ornamentation, experimental manipulation of the quality of male ornamentation of wild 
individuals would be necessary. Because a test of the handicap model is beyond the scope 
of this study, I do not discuss the predictions of this hypothesis further. However anecdotal 
evidence addressing this hypothesis is presented in the discussion. 

Since parasites are a ubiquitous problem for wild turkeys, the Hamilton and Zuk 
(1982) theory of mate choice as an adaptation against parasitism seems a plausible 
explanation for the maintenance of FS in this species. If turkey hens are using male 
ornamentation to assess parasite burden, the intensity of infection by the most deleterious 
parasites should be inversely correlated with the quality of male ornamentation that females 
are using to choose a mate. To be favored by females, these ornaments should be better 
indicators of parasite burden than other anatomical structures, such as bill or tarsus length. 

Adult male wild turkeys begin their energetic courtship displays in early spring, 
often while snow remains on the ground, relying on their fat reserves for sustenance 
(Pelham & Dickson 1992). If the ability to access food and store energy for surviving 
winter snow storms is an important determinant of survival as previous research suggests, 
females may use the quality of a male's display as an indication of stored energy reserves. 
If this is the case, female choice should rely heavily on the most energetic parts of the male 
display and on any other characters that might be indicative of fat reserves, such as body 
condition. 



30 

Age is perhaps the most honest indicator of good genes. Males that survive despite 
parasites, predators, and food shortages have demonstrated their superior ability merely by 
remaining alive. Thus females may choose mates based on ornamentation that reliably 
reveals male age. Although beard length and body weight are positively correlated with age, 
spur length is thought to be the best indicator of yearly age classes in eastern wild turkeys 
(M g. silvestris : Kelly 1975; Steffen et al. 1990). This suggests that females should choose 
to mate with males with longer spurs. 

The arbitrary preference models for the evolution of male ornamentation predict no 
relationship between ornamentation and male survival or condition. If the characters chosen 
by females are not related to any of the factors that limit turkey survival or fecundity, it 
seems reasonable to conclude that they are maintained purely by the increased mating 
success of the male without any direct increase in the reproductive success of the female. I 
test these hypotheses for the maintenance of ornamentation in wild turkeys with 
experimental data collected from captive mate-choice trials and correlational data collected 
from wild caught males. 

Methods 

Study Species 

Day-old wild turkey poults were purchased in May 1991 from a gamefarm (L&L 
Pheasantry, Hegins, PA, USA) whose large breeder flock continued to experience gene flow 
from wild males (M g- silvestris ) until a decade ago. Poults were raised indoors under 
heat lamps with gamebird starter feed (Purina Startena, 30% protein) and water provided M 
libitum . After eight weeks the birds were transferred to a large (5.3m x 5.3m x 2.6m) 
outdoor pen at the Florida Museum of Natural History's Special Projects Laboratory. 

After 14 weeks of age, males were maintained separately from the females in two 
visually isolated groups of 16 in sand-floored aviaries (5.3m x 5.3m x 2.6m). Females 
were moved to a cement-floored pen (5m x 12m x 4m) that was visually isolated from the 



31 

males. To minimize wastage only as much feed (Purina Grower or Maintenance, 19 or 12% 
protein) as could be consumed in 3-4 hours was provided daily, varying seasonally. 
Additionally a variety of green forage (e.g., cut grass, bamboo leaves, etc.) was provided 
twice a week. Water was available ad lib. 

Very limited displaying observed during pilot studies in early 1992 was attributed to 
suppression by dominant males in the relatively crowded, group housing. To alleviate this 
problem all males were housed individually in cylindrical wire cages (1.3 m in diameter and 
lm high) at 15 months of age. Black plastic dividers prevented males from physically 
interacting with males in neighboring pens, although they could see and hear other males in 
pens 4 m away. Each male was fed approximately 0.5 1 of breeder rations (Purina Layena, 
20% protein) daily, along with occasional peanuts, wild bird seed, or carrot or apple slices. 
Water was provided in 0.5 1 containers and was replaced daily. 

Mate Choice Experiments 

To investigate how wild turkey ornamentation may have evolved by female choice it 
is necessary to test the assumptions and predictions of the good genes and arbitrary 
preference models. First do females mate randomly with respect to male traits, and if not, 
which traits do they assess in prospective mates? Second are the characters assessed by 
females particularly good indicators of the male's success in dealing with factors limiting the 
fitness of wild turkeys? 

The mating preferences of female wild turkeys were tested in two experiments. In 
the Live Male experiment, females were given a choice between two naturally displaying 
males. The characteristics of males chosen by females were compared to the characteristics 
of males not chosen by females to identify the characters correlated with female choice. The 
Male Model experiment gave females a choice between two artificial males that differed 
only in the amount of head ornamentation. The model experiment ensures that the character 



32 

thought to be assessed by females in the live male experiment is not merely the correlate of 
another unmeasured character actually under assessment by females. 
Live male experiment 

Live males . Thirty-three, 20-month old males were exposed to an artificial 
photoperiod of 14 hours for four weeks prior to and during the mate choice tests. Prior to 
the mate choice trials, males were classified as "displayers" or "nondisplayers" based on 
whether they strutted consistently during a half hour observation period on each day of the 
week before the first trials. During the trials no "nondisplayers" became "displayers," but 
the reverse was true. The 1 1 males classified as consistent displayers were used in the mate 
choice trials. Seven ornamental characters were measured prior to the first trial. Relaxed 
snood length was measured from the point of attachment at its base to the tip with a small 
ruler. The snood was measured again after being stretched by attaching a clip to the tip of 
the snood and pulling on the clip with a Pesola scale to a tension of 30 g. The maximum 
vertical and horizontal diameter of each frontal caruncle, as well as its thickness, was 
measured with a ruler. The radii of the frontal caruncles was converted to an approximation 
of total caruncle area using the equation for the area of an ellipse (A=abrc). The red, polyp- 
like projections on the neck called side caruncles were counted. The width of each half of 
the thickened, whitish skullcap was measured by placing the ruler in a line from the most 
posterior point at which the skullcap halves meet along the middle of the cranium to a point 
dorsal to the middle of the eye. The beard was measured from where the "hairs" leave the 
skin to its greatest length. Briefly, tarsal spur length was measured from where the spur 
enters the scaled skin to the distal tip (Kelly 1975). Tarsus length was measured from the 
articulation of the tarsometatarsus with the tibiotarsus to the third scute of the central 
phalange of the foot Weight divided by tarsus length was used as an index of male body 
condition and is referred to as such or merely as male condition. 



33 

Females . Twenty-three, 20-month old female wild turkeys were exposed to an 
artificial photoperiod of 14 hours for four weeks prior to, and during, the mate choice tests 
in January-March 1993. 

Experimental design . The large cage used for housing the females was subdivided 
into three sections to serve as a mate choice arena (Figure 3-2a). The female flock was 
housed in one half of the aviary during the experiment Each female was admitted singly to 
the choice area through a door in the opaque plastic barrier that prevented the untested 
females from seeing the displays of the males or the choices made by subject females. An 
additional opaque barrier prevented the males from directly interacting with one another. 
The subject female was separated from the males by hardware cloth that had been painted 
black to make it less visible. Each female was tested only once and was presented with a 
unique pairing of males that was never presented to any other female. In total 1 1 males 
were used 2-4 times each (mean= 3.3); there was not a significant correlation between the 
number of times each male was presented and the frequency of female choice (Spearman 
Rank Correlation, r s =0.51, P= 0.14). Males were assigned to the two display areas 
randomly on the afternoon before the trial. Only one trial was conducted in any 24 hr 
period from 14 Jan-12 March 1993, between 08:00-16:00 hrs. During the ten minute pre- 
trial period before the female was admitted, the frequency of spontaneous strutting by each 
male and the degree of snood distention (on a scale of 0-4) were recorded. Snood 
distention was recorded again immediately after the female was admitted and strutting 
frequency was recorded until the female solicited one of the males. Females revealed their 
choice of mate by "crouching" (Healy 1992a), a conspicuous mating solicitation posture 
exhibited in front of the chosen male. The time spent by the female in front of each male 
was also recorded until solicitation. Trials in which females did not solicit within 30 min 
were excluded from analysis. The two males from a failed trial were tested again with a new 
female the next day. 



34 



Holding Area 



FEMALE 



Live Male 1 



Live Male 2 



B 



Male Model 1 



Male Model 2 



FEMALE 



Figure 3-2. Mate choice arenas. A) Female is admitted from a holding 
area to the choice area where she has a choice of two displaying males; B) 
A female is given the choice of soliciting one of two artificial males that 
differ only in their snood length and side caruncle number. Screen divider 
between males and female is represented by thin line. 



35 

Data analysis . The characters correlated with female mate choice were determined 
by comparing the characteristics of the male solicited with those of the male not solicited in 
each trial. Wilcoxon matched pairs signed-rank tests were used with characters that were 
independent of other characters (Siegel, 1956). However some of the measurements of 
male ornamentation covaried strongly with each other and with tarsus length (Table 3-1), 
making it difficult to tease apart the relative contribution of these characters to mate choice. 
Principal component factor analysis was used to isolate independent axes of variation in the 
correlation matrix of the five most highly covarying characters (tarsus length, spur length, 
skull cap width, stretched snood length and frontal caruncle area). Frontal caruncle area was 
transformed by log (x) °- 5 when combined with linear measurements in the factor analysis. 
Subsequently these axes were transformed (i.e. rotated) using the varimax solution to 
generate four orthogonal axes on which the variables were loaded as uniquely as possible 
(Table 3-2). These axes provided four sets of independent axis scores, each set composed 
largely of only one character unlike the strongly covarying raw data, that could be used to 
determine which of these five characters was most important to a female's choice of males. 

For each trial the differences between the scores of the males presented to the female 
were calculated by subtracting the score of the male not chosen from that of the male that 
was chosen. If females chose males at random with respect to these characters, the 
distribution of the differences between preferred and not preferred males would be expected 
to have a mean of zero. A positive mean is expected if females are choosing males with the 
larger or greater forms of these characters as hypothesized. Because females were used 
only once, male pairings were unique in every trial and the difference between male 
characters was used in the analyses. This means that each trial was independent despite the 
fact that most males were used more than once. Data analysis utilized the "Spin" abilities of 
SASjmp (SAS Institute Inc. 1989) and the general statistics of Statview (Abacus Concepts 



36 






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Inc. 1986). Where appropriate, mean values in the results are followed by the standard 
error of those measurements. 
Male model experiment 

Male models . Each female was admitted singly to an arena (Figure 3-2b) in which 
she had a choice of interacting with either of two artificial males modified from plastic 
hunting decoys of hens. These models were altered in the following ways to make them 
appear like strutting males. The heads of the two decoys were painted simultaneously with 
alternating brush strokes of enamel paint so that they resembled one another as closely as 
possible. The skullcap was painted a light blue, the orbital area a dark blue, the dewlap and 
throat were painted red, the sides and back of the neck were painted pink with narrow red 
rings applied around the circumference. Natural beards were removed from two domestic 
turkey gobblers. Each beard was divided in two, with equal numbers of "hairs," and then 
these were trimmed to 17 cm in length and applied to the models. 

The decoys have a closed tail, typical of a resting bird. However strutting males 
have a fanned tail. Two artificial fans were constructed from colored poster board, glue and 
black permanent marker. The vertical diameter of the tail was 33 cm and the horizontal 
radius was 69 cm. The fanned tails were positioned just behind the wing tips of the decoys 
and held in place from behind with two thin wooden dowels that were stuck in the ground to 
stabilize the tail. The models themselves were mounted on a wooden dowel so that their 
backs were at a height of 0.65 m. Strutting turkeys drag the primary feathers of their wings 
on the ground, but I made no attempt to simulate this posture; the models had their wings in 
the normal resting position on their sides. 

To provide the sound of strutting, a recording of a single strut from a commercially 
available video (Griffen Productions 1990) was played back alternately between the males 
so that each male model "strutted" four times per minute. One small 5 watt speaker was 
placed to the side and behind each male and aimed towards the area immediately in front of 
the male. Using the individual volume controls on the speakers and a Tandy sound meter, I 



38 

was able to ensure that the amplitude of the struts were equal (73 db) at a point 0.75 m 
immediately in front of each male. 

The male models were identical in coloration, tail size, beard length and display 
frequency. To test whether the most variable types of fleshy head ornamentation seen in 
live males affect mate choice, it was necessary to construct artificial snoods and caruncles 
for the artificial males. Four snoods (two 4.0 cm long, two 6.6 cm long), 14 side caruncles 
(1.2 cm x 1.9 cm x 1 cm) and four frontal caruncles (2 cm in diameter) were constructed 
from latex caulking. The snoods were painted as above so that they were bluish pink, the 
caruncles of both types were painted red. These were applied with small pieces of double- 
sided tape so that one male model was "more ornamented", i.e. given a long snood coupled 
with 5 caruncles on each side of his neck, while the "less ornamented" male was given the 
shorter snood and only two caruncles on each side of his neck. Both males had two frontal 
caruncles placed side by side at the base of the front of their necks. Only snood length and 
side caruncle number were varied because these characters were the most variable in wild- 
caught males. One or more of the bodies, tails, beards, snoods or caruncles were exchanged 
between the models after each trial and the position of the more ornamented male was 
randomized. Thus female preference could be attributed to the only consistent difference 
between the males: snood length and side caruncle number. 

Females . Twenty-three 17-month old female wild turkeys were implanted with a 21 
day-release pellet of 25 mg of estradiol (Innovative Research of America, Toledo, OH, 
USA) on 3 Dec. 1992. After 10 days, when most females were exhibiting sexual behavior, 
mate choice trials were conducted. 

Experimental design. Male model trials were conducted between 08:00-16:00 h 
from 13 Dec-15 Dec 1992. The playback of the strut recording was started before each 
female was admitted singly to the arena via a remotely opened door. Starting the moment 
the female stepped into the middle of the arena from the waiting area, I recorded the amount 



39 

of time she spent in each model's half of the arena. A trial ended when the female solicited 
or after 20 min had passed. Each female was tested only once. 

Data analysis . If females chose mates at random with respect to male snood length 
and caruncle number, an equal number of more ornamented and less ornamented males 
should be solicited. However if females prefer males with the more elaborate form of these 
traits, the more ornamented male should be solicited significantly more often. A Binomial 
test (Siegel 1956) was used to test the statistical significance of the results. 

Correlates of Ornamentation in Wild Males 

Free-living male wild turkeys were captured and measured to determine if male 
ornamentation serves as a good indicator of male viability. Yearling male wild turkeys were 
captured with bait drugged with alpha chloralose (Williams & Austin 1988) at Paynes 
Prairie State Preserve in Alachua Co., Florida, USA between February and March of 1991 
and 1992. Ornamentation was measured as described above for captive males, with the 
exception of skullcap width, which was not measured. Drugged birds were kept indoors in 
boxes specially designed for transporting wild turkeys until they had recovered sufficiently 
for safe release (24-96 hr). 

The number of attached ticks on the head and neck and on the undersides of both 
wings were counted. In addition the lice on the feathers of the chest, back and rump were 
counted by lifting and scanning the feathers of each region for two minutes. Blood smears 
were made from each individual using blood collected with a heparinized capillary tube from 
the alar vein. The smears were air dried, fixed in 100% methanol, and stained. Blood 
parasite burden was measured as the number of blood cells infected with hematozoa seen 
per 30 minutes of scanning under oil immersion at lOOx. Fecal samples were collected 3x a 
day from the boxes of the recovering birds. One gram from each sample was mixed with 
20 ml of a saturated NaN03 solution and filtered through cheese cloth into a centrifuge 
tube. The tube was filled to the very top so that a coverslip placed on the tube opening 



40 

would remain adhered there during the subsequent 5 minutes of centrifugation at 1500 rpm. 
During centrifugation most parasite "eggs" either float to the top and adhere to the coverslip 
or sink to the bottom, depending on their specific gravity. After centrifugation the coverslip 
was placed on a microscope slide and thoroughly scanned. Parasite eggs were identified 
and counted directly or when present in very large numbers, estimated with the use of a 
McMaster's slide. There are at least 6 species of eimerian coccidia that infect turkeys 
(Davidson & Wentworth 1992). Unfortunately, these species are difficult to identify and 
could only be categorized as having large or small oocysts in this study. The sediment of 
each centrifuge tube was throughly examined for trematode and other eggs under a 
dissecting microscope. 

Additional measures of ornamentation and blood smears were collected from eight 
hunter-killed wild turkeys at Camp Blanding Wildlife Management Area, Florida, in March 
1990. 

Results 
Live Males Experiment 

Eighteen of the 23 females tested signalled their choice of mates by soliciting 
copulation from one of the two males presented in each trial. Traits of males solicited and 
not solicited are compared in Table 3-3. Females strongly preferred males with 
comparatively higher scores on the second rotated component, i.e. those with longer snoods 
and wider skullcaps (unpaired t-test, one-tailed, v =17, mean=1.01, t=3.65, P=0.001). The 
length of the male's snood during display, the character state actually visible for assessment 
by females, was strongly correlated with the relaxed and stretched snood measurements 
(r s =0.80, n=l 1, P=0.01; r s =0.75, n=l 1, P=0.02, respectively). The other variables that 
loaded on the first, third and fourth axes: tarsus length, frontal caruncle area and spur length, 
respectively, did not account for female choice of males (t-tests, one-tailed, P>0.05). 
Characters analyzed individually, i.e. pre-trial strut rate, trial strut rate, 



41 



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42 

male condition, frontal caruncle depth, side caruncle number, and beard length, also did not 
explain female mating preference (Wilcoxon signed rank tests, P»0.05). In the live male 
trials females spent significantly more time with the male that they solicited (1.7 ± 0.72 min 
for the chosen male vs. 0.42 ± 0.17 min for the male not chosen; Mann- Whitney U-test, 
ni=17, n2=17, U=74, U ! =215, P=0.02). The mean time until solicitation was 2.1 ± 0.85 
min. Time until solicitation was not dependent on the similarity of the scores or measures 
of any of the variables of the two males (Spearman rank correlation, P>0.05). The three 
females who did not choose the male with the higher of the two scores for the second factor 
seemed to mate more quickly on average than females who did (1.0±0.8 min vs. 2.3±1.0 
min). 
Male Models Experiment 

Of the 23 females tested in the male model trials, only nine solicited copulation from 
the decoys. One female solicited immediately in the center of the entrance way of the arena 
and thus her choice was ambiguous and this trial was excluded. Of the eight remaining 
females, who clearly solicited on only one side of the arena, seven solicited before the more 
ornamented model. This preference for the more ornamented model was statistically 
significant (Binomial Test, one-tailed, P=0.035). Six of the eight females spent more time 
with the model male that they subsequently solicited; however, this difference is not 
statistically significant (Binomial Test, one-tailed, P=0.145). The two females who did not 
spend more time with their preferred male also took much longer to choose (mean= 9 min 
vs. 1.7 min, overall mean= 4 min). Three of the females that chose the more ornamented 
model never spent any time on the side of the less ornamented decoy. The single female 
that solicited the less ornamented decoy never visited the more ornamented model but 
solicited in a typical amount of time (1.88 min). 

Nine of the 14 nonsoliciting females were obviously distressed, as evidenced by 
frequent alarm calling or frantic attempts to exit the arena, despite a training period. These 
females showed no preference for either side of the arena (Binomial Test, two-tailed, 



43 

P=0.5). The remaining five females who neither solicited nor alarm called engaged in 
nonsexual behaviors such as dust-bathing or preening. They also showed no preference for 
either half of the arena (Binomial Test, two-tailed, P=l). 

Correlates of Ornamentation in Wild Males 

Nine yearling male wild turkeys were captured, measured and screened for parasites 
(Table 3-4). All males sampled for these ectoparasites (7 of 9) had attached ticks 
(Argasidae and Ixodidae). Ticks were most common on bare areas along the alar vein under 
the wing, but also occurred on the back of the head. The total tick burden was not 
significantly correlated with any measure of male ornamentation or body size (all P >0.05). 
The number of ticks attached on the head, however, was positively correlated with the 
relaxed length of the snood (r s = 0.7, n= 9, P=0.05). Lice were most common on the rump 
(only one of seven males had no rump lice) but were not correlated with male ornamentation 
(all P> 0.05). Half of the eight males sampled for back lice were infected. Numbers of lice 
on the back were significantly negatively correlated with the number of side caruncles on 
males (r s =-0.66, n=8, P=0.03) and showed a similar trend with the length of the tarsal spurs 
(r s =-0.53, n=8, P=0.07). Total lice numbers were not correlated with any measure of male 
ornamentation, size or condition (all P»0.05). 

One to five fecal samples were collected from each bird (mean=3.4±0.6). Fecal 
analysis revealed two parasites to be common: a protozoan coccidia (Eimeria spp.) and a 
cecal nematode (Trichostrongvlus tenuis) . Eggs from an unidentified cestode were also 
detected in one fecal sample flotation. Sediments from the fecal samples appeared 
completely free of parasite eggs. 

All nine males had infections with the large coccidia and eight of nine were infected 
with small coccidia. Eimeria burdens were not negatively correlated with tarsus length, mass 
or condition (all P» 0.05). However coccidia burden was negatively correlated with some 
measures of male ornamentation. Average burdens of the large eimerian were 



44 



Table 3-4. Parasite loads of one-year-old, wild caught, male wild turkeys. 

Parasite % Occurrence (N) Mean Load (±SE) 

ticks 

head 100 (9) 8.4 (±3.8) 

wing 100 (9) 17.3 (±3.5) 

total 100 (9) 25.8 (±5.9) 

lice 

back 50 (8) 2.0 (±1.0) 

rump 86 (7) 6.8 (±2.3) 

total 100 (7) 7.0 (±2.8) 

Eimeria oocyts 

large 100 (9) 342.2 (±190) 

small 89 (9) 2276.2 (±2042) 

total 100 (9) 2618.4 (±2214) 

Trichostrongylus eggs 

total 56 (9) 22.3 (±14.81) 

Blood Parasites 

Haemoproteus 86 (7) 7.3 (±2.5) 

Leucocytozoon 14 (7) 0.1 (±0.1) 

Plasmodium 43 (7) 0.6 (±0.3) 



45 

significantly negatively correlated with the relaxed snood length of males (r s =-0.78, n=9, 
P=0.03). Average burdens of the small eimerians showed a similar, though nonsignificant, 
negative trend with relaxed snood length (r s =-0.63, n=9, P=0.07). The overall average 
coccidia burden showed a very strong significantly negative correlation with relaxed snood 
length (r s =-0.84, n=9, P=0.02). 

Individuals with extremely high burdens of coccidia in one sample (e.g., tens of 
thousands) never had samples with very low numbers of oocysts. Individuals with lower 
burdens (e.g., hundreds of oocysts) generally had at least one sample in which no or few 
oocysts were detected. It appears that heavily infected animals are subject to a more chronic 
and potentially more debilitating release of oocysts from the gut than are animals with lower 
infections, perhaps because more species of coccidia are causing the infection. If this is the 
case, perhaps the minimum sample is a better indicator of susceptibility. Relaxed snood 
length was not more strongly correlated with the lowest (or highest) burden sampled than 
with the average total burden, although these measures were significantly or nearly 
significandy negatively correlated with relaxed snood length (r s = -0.55 to -0.82, n=9, 0.02 
<P> 0.09). Stretched snood length on the other hand was not significandy associated with 
average coccidia burden but was significantly negatively correlated with the lowest 
measurements of the large, small and total eimerian burdens (r s = -0.66, -0.70, -0.70, 
respectively; n= 9, P< 0.05). Also there were nonsignificant negative trends in correlation 
between large, small and total lowest coccidia burden per male and frontal caruncle area (all 
r s = -0.63, n=9, P=0.06) and between lowest burdens of small coccidia and frontal caruncle 
depth (r s =-0.74, n=8, P=0.06). The tendency of some ornaments to be correlated with the 
minimum sample burden suggest that this may be a more sensitive measure of parasite 
burden than average or maximum burdens. 

The thread nematode fTrichostrongvlus tenuis ) was present in five of the nine males 
sampled. Average nematode egg burdens were not correlated with male ornamentation, 
body size or condition. 



46 

Data from hunter-killed animals showed that relaxed (Mann- Whitney U test, U=0, 
U!=16, ni=4, n2=4, P=0.03) or stretched (Mann-Whimey U test, U=0, U!=12, ni=4, n2=4, 
P=0.03) snood length could be used to distinguish between first year and older males. 
Over the three year classes measured, relaxed snood length increased significantly (rho= 
0.79, n=8, P= 0.04) but stretched length only showed a nonsignificant trend (rho= 0.71, 
n=8, P= 0.09) with age. These correlations became nonsignificant when the effects of body 
condition were removed by partial regression. However relaxed snood length remained 
strongly correlated with male condition if the effects of age are removed (rho=0.56, n=13, 
P=0.05). 

Discussion 

The results provide support for a parasite-driven explanation for the maintenance of 
female choice for male ornamentation in wild turkeys (Hamilton & Zuk 1982). They do not 
support the arbitrary preference model. Females preferred to mate with males that had 
longer snoods and broader skullcaps; two tightly covarying male traits. Although skullcaps 
were not measured on wild individuals, stretched and relaxed snood length were longest in 
individuals with lower and less chronic burdens of coccidian oocysts. Surveys in the wild 
have shown this parasite to be quite widespread; 46-100% of turkey poults are infected and 
40% of droppings collected from adults contain oocysts (reviewed by Davidson & 
Wentworth 1992). Perhaps because this parasite is often ignored during searches for 
internal parasites (Ruff et al. 1988), coccidiosis is not commonly suspected to contribute to 
the mortality of adult wild turkeys. However laboratory transmission of Eimeria from wild 
individuals to domestic poults proves these parasites have the potential to be highly 
pathogenic (Prestwood et al. 1973). Chronic effects of coccidiosis in domestic poultry 
include delayed maturation due to decreased plasma testosterone levels (Ruff 1988), 
decreased egg and sperm production and lower fertility (Bressler et al. 1951; Ruff et al. 
1984; Ogbuokiri & Edgar 1986; Ruff & Wilkins 1987). If similar effects occur in wild 



47 

populations, and if resistance to coccidia in wild turkeys is heritable as it is in domestic 
poultry (Johnson & Edgar 1982), females that choose mates that are resistant to Eimeria 
would have greater fitness because their offspring are relieved of the deleterious effects of 
these parasites. Thus female choice for male snood length appears to be a behavioral 
adaptation against parasitism. 

The beard, frontal caruncles and other aspects of male ornamentation were not 
subject to female choice, despite the fact that there is some indication that they may also 
indicate parasite burden. Why did females not discriminate among males by these 
characters? There are three possible explanations. First and most obvious, is that the captive 
turkeys of the eastern subspecies are not subject to the same selective pressures as the wild 
osceola males sampled in Florida. Limited data suggest that parasite burdens may be lower 
in the northern parts of the wild turkey's range (Sasseville et al. 1988) Second the apparent 
trends between caruncle quality and other parasites may be the spurious result of using 
multiple statistical tests. Larger sample sizes of wild males are needed to document the 
reliability of these other ornaments as indicators of parasite burden to females. Last, studies 
of female choice in other galliformes have shown year to year shifting in some of the male 
characters that are assessed (e.g., Zuk et al. 1992), suggesting that frontal caruncles, which 
appear to be inversely correlated with parasite burden, may be important in mate assessment 
in other years. 

Threadworms, Trichostrongylus. have a dramatic effect on the fitness of some other 
galliforms, particularly grouse (Hudson & Dobson 1991), but infections in wild turkeys are 
generally not severe enough to cause pathologies (Davidson & Wentworth 1992) and 
therefore it was not surprising that these nematodes did not affect the degree of male 
ornamentation. Similarly ectoparasite burdens were low and probably have a subde, 
cumulative effect on male condition not readily revealed by ornamentation (e.g., Booth et al. 
1993). 



48 

Because harsh winters limit survivorship in wild turkeys, it was hypothesized that 
females should try to assess male ability to survive such conditions. It was hypothesized 
that turkey hens could assess male condition by the male's ability to perform energetically 
costly displays. This hypothesis was not supported directly. Male condition and display 
frequency during the mate choice trial did not explain variation in female choice. In fact 
some females solicited so quickly that they would have had little opportunity to measure 
male strut frequency. However the characters females assessed during mate choice, snood 
length and skullcap width, were positively correlated with the male's average strut frequency 
over all his trials (Table 2-1). In the well-fed captive turkeys neither average strut frequency, 
relaxed or stretched snood lengths nor display snood length were correlated with male 
condition. But after statistically removing any effects of age, the stretched snood length of 
wild males was significantly positively correlated with male condition and age was no 
longer correlated with snood length. Although male strut frequency was apparently not 
assessed by females during the mate choice trials, females mated with males that strutted at a 
higher rate and that were in better condition by choosing males with longer snoods and 
wider skullcaps. Further field captures and experimental manipulations will be necessary to 
determine if display rate is a specific indicator of the stored fat resources of the male. 

Male age is perhaps the best indicator of a male's good genes. Older males are 
probably not a random sample in terms of natural selection; they have survived multiple 
challenges over time, including parasitism, starvation and predation. One hypothesis for the 
maintenance of male ornamentation in wild turkeys is that these characters serve as 
indicators of male age. In this study captive females did not choose among 2 year old males 
based on previously documented age class indicators, such as spur length. This may be 
because these cues provide no information when males are very similar, i.e. within one age 
class. Unfortunately previous studies of correlates of wild turkey age have ignored the head 
ornamentation of males (Kelly 1975; Steffen et al. 1990). Results from a limited sample of 
wild males covering three age classes shows that the characters females are assessing in 



49 

mate choice are not good indicators of male age because age covaries with body condition. 
A larger sample size is needed to tease apart these two variables. For example, more field 
data are needed to determine if the snood lengths of heavily parasitized, older males are 
shorter than lightly parasitized, younger males. In any case snood length within one age 
class appears to be a reliable cue to the body condition of the bearer as well as to the 
coccidia burden among males. 

The handicap model for the maintenance of male ornamentation proposes that 
females assess a male's ability to survive despite his burdensome ornaments. Field 
experiments that record the reproductive success and survivorship of manipulated males are 
necessary to test this hypothesis. Nevertheless anecdotal observations provide some 
support for the handicap model. The conspicuous ornamentation and courtship displays of 
male wild turkeys attract predators and are thought to increase their risk of predation (Miller 
& Leopold 1992). The uninsulated bare head of males may also represent a 
thermoregulatory handicap. Birds generally lose large quantities of heat from feathered 
heads (Hill et al. 1980). Unfeathered heads such as the turkey's should lose even more heat 
and may hasten male starvation during severe winter storms. Since there is no clear 
advantage to having bare heads in winter, it seems reasonable to suggest that the bare heads 
of male wild turkeys may have evolved as a handicap. Similarly other forms of male 
ornamentation, such as the beard and fanned tail, might serve as handicaps. 

This study suggests that the snood and skullcap of males are maintained by female 
choice for males with low burdens of coccidia. Also these traits may be used by females to 
choose older males as mates and perhaps males that have more body fat Snood length and 
skullcap appear to be the only aspects of male ornamentation under direct selection by 
females. The selective pressures maintaining the striking array of extravagant 
ornamentation of wild turkeys is only partly explained. Males have strikingly colored 
caruncles on their head and neck, a long beard projecting from their chest, iridescent 
feathers and a large fan-like tail that are apparently not subject to female choice, but may 



50 

instead play a role in male-male competition (Chapter 4) or be maintained because of its 
other functions (Chapter 5). 



CHAPTER 4 

MALE DOMINANCE AND VARIATION IN 

FLESHY HEAD ORNAMENTATION IN WILD TURKEYS 



Introduction 

The mating system of wild turkeys has been classified as male-dominance polygyny 
(Williams & Austin 1988). In the breeding season males vocalize ("gobble") to attract 
flocks of receptive females and then follow and display to those hens throughout the day. 
During this time other males may be attracted to the same females and battles between males 
over mating access often result (Watts & Stokes 1971). Because males are unable to obtain 
exclusive access to females by defending food or other resources that female turkeys need 
(Emlen & Oring 1977; Hurst 1992), they control access to the females themselves. As a 
result male wild turkeys engage in frequent, direct, agonistic interactions that determine 
mating success (Watts & Stokes 1971). These agonistic interactions begin when the males 
are juveniles and establish dominance heirarchies within their age cohort (Healy 1992a) and 
continue as males encounter and fight with other males after dispersal from the natal 
territory and in subsequent breeding seasons (Watts & Stokes 1971; Williams & Austin 
1988; Healy 1992a). 

The War Propaganda model (Fisher 1958; Borgia 1979) proposes that in mating 
systems such as the wild turkey's, in which females gain no direct benefits from males and 
males compete for access to females, male fighting success should be assessed by females 
during mate choice. Females should do this because fighting ability is probably a good 
measure of overall male condition. Another reason to mate with dominant males is that the 
components of dominance may be heritable (Dewsbury 1990); therefore, a female that 
mates with a dominant male may have higher fitness because of an increased likelihood that 



51 



52 

her mature male offspring will be able to gain access to hens. But females are not the only 
sex in which selection should favor the ability to recognize dominant males. To avoid 
battles in which the risk of injury outweighs gains in lifetime fitness, males should assess 
the condition of their competitors before fighting. Both the receiver and the signaller might 
benefit from the transmission of information about male condition (Rohwer 1975; Rohwer 
1977). Dominant males avoid the costs of continually battling weaker males for preferential 
access to resources and subordinate males avoid the risk of serious injury from dominant 
males who are likely to be healthier and stronger and win fights (M0ller 1987). Thus both 
females and males should assess the dominance status of males. 

Fleshy ornaments are associated with intrasexual competition in many galliform 
species (Stokkan 1979; Brodsky 1988; Ligon et al. 1990; Holder & Montgomerie 1993) 
and are uniquely suited to signal male status honestly. These structures generally develop 
only upon sexual maturity and their size in males is known to be testosterone dependent in 
some species (Allee et al. 1939; Collias 1943; Stokkan 1979). Higher testosterone levels 
are often associated with dominance and increased aggressiveness in birds (Wingfield et al. 
1987), suggesting that fleshy ornamentation may correlate with a male's dominance status. 
Dominant males might have relatively higher testosterone levels because they are in better 
physical condition (Ligon et al. 1990) or because they are able to suppress the testosterone 
levels of subordinate males (Lisano & Kennamer 1977). 

As demonstrated earlier (Chapter 3), the snood length of male wild turkeys is a 
indicator of coccidia burden, condition and possibly age. This would suggest that males 
could use this aspect of male ornamentation to assess the vigor of males they encounter and 
thus consider the risks of combatting those males. If this is the case, males with longer 
snoods would be expected to be dominant over less ornamented males, and that males with 
similarly sized ornamentation should be in the most conflict over relative status. In this 
study I test this hypothesis by comparing the ornamentation of males matched in dyadic 
dominance trials. However males may establish dominance not because of ornamentation 



53 

itself, but because of strongly correlated attributes such as body weight Therefore I also 
examine the response of captive males to the presentation of artificial males that differ only 
in snood length and caruncle number. 

Methods 

A detailed description of the rearing of the wild turkeys used in these experiments, 
including cage sizes is provided in the previous chapter (Chapter 3). Briefly, the wild 
turkeys were obtained from a game farm as day-old chicks. At four months of age the 
females were separated from the males and the males were divided into two, visually isolated 
groups. Pilot observations during the spring 1992 breeding season showed that very few of 
the males actively strutted when group housed. Therefore when the males were 15 months 
old, six months before the 1994 season, the males were moved to individual pens separated 
by opaque dividers. This had the effect of stimulating more males to perform the strut 
display. Eleven of the 28 males displayed spontaneously and regularly in their individual 
pens. These animals were designated "displayers" and were used in the mate choice trials 
(described in Chapter 3) before being tested in the dominance trials. For the dominance 
trials, conducted in Feb-April 1993, a male from one rearing flock was matched with a male 
from the other flock. These males were chosen from their respective flocks at random 
except that "displayers" were always matched with other displayers. An additional male 
who displayed occassionally was used in the dyad with the odd numbered "displayer". The 
pairing of males based on display frequency mimics the situation in the wild where 
displayers usually fight one another and are avoided by nondisplaying individuals and 
juveniles (personal observation). Each dyad of males was measured for ornamentation and 
body size, as described previously (Chapter 3), on the day before the dominance trial. 



54 

Live Males 

In the live male dominance trials, two males were admitted to a central arena (2.7m x 
5.3 x 2.7m) from their respective holding pens (Figure 4- la). The males were familiarized 
with the arena for several hours on the day prior to the trial and had spent part of their 
rearing period in the pen as well. No food or mates were provided in the arena, although the 
males often found something to peck at on the dirt floor of the pen. This situation 
simulated a random meeting of unfamiliar males on common ground with no resource to 
contest. Trials lasted 10 minutes and were videotaped so that the rapidly occurring 
dominance interactions could be reviewed and transcribed later. 

A heirarchy of criteria was used for designating one member of the dyad as 
subordinate and the other dominant Most males actually fought with one another. 
Fighting begins when one male approaches the other and begins giving "fighting purrs", 
vocalizations that elicit combat (Healy 1992a). The other male typically responds with 
fighting purrs until one of them slaps the other with a wing while simultaneously kicking 
him. The birds continue to wing slap and kick one another until one of them suddenly turns 
and attempts to flee. Fleeing males are generally pursued and sometimes pecked on the 
head. If the males fought, the fleeing male was designated the subordinate. In some trials 
one male fled immediately upon encountering the first male and as a result was designated 
the subordinate. In one trial the males did not fight nor did one flee from the other. In this 
case the male that was displaced while pecking at the ground was designated the 
subordinate. 

For each trial I recorded the number of wingflapping bouts given by each bird prior 
to physical contact (pecking in the absence of fights, or wing slapping/kicking in birds that 
fought) and latency to physical contact. A wingflapping bout consisted of the male standing 
in place and flapping the wings two to five times. This action pattern is often used in 
aggressive contexts in Galliformes (Kruijt 1964; Buchholz 1989). If the males fought I 
recorded the identity of the male who began giving "fighting purrs", the frequency of 



55 




Male in 
Waiting 



8- 



2. 



to l- 



B 




live 

Male 



Figure 4-1. Male dominance trial arenas. A) Randomly matched males 
are admitted to a central arena from holding pens; B) A living male is 
given the choice of feeding from in front of two artificial males of 
different snood lengths and side caruncle numbers. Another male waits in 
a holding area. 



56 

pecking and kicking by each male during combat, the duration of the fight and the identity 
of the male that stopped fighting first and began to flee. A dark shelter was provided in the 
rear of the arena so that the subordinate male could hide from the aggressor. None of the 
males was injured. 

The characteristics of the dominant male were compared with those of the 
subordinate in each trial with one-tailed Wilcoxon matched pairs signed ranks tests (Siegel 
1956) or one-tailed, unpaired t-tests on principal component factor score differences. The 
differences between the factor scores of the two males used in each trial, calculated as the 
dominant male's scores minus the subordinate male's scores, are expected to be significantly 
greater than zero if dominant males are more highly ornamented (as described in the 
methods for Chapter 3). Correlations between time measurements and differences in male 
ornamentation were determined using the Spearman rank correlation coefficient 
Differences in ornamentation between subgroups of males, e.g., displayers and 
nondisplayers, were tested for statistical significance with the Mann-Whitney U test. 
Male Model Trials 

Artificial males constructed from decoys were used to test the effects of male fleshy 
ornamentation on the decision-making of live males. The use of models allowed for the 
experimental control of male characteristics that usually covary with snood length. The 
model males were exactly like those used in the mate choice experiments described earlier 
(Chapter 3), except that they did not have fanned tails and they were not accompanied by the 
recorded display sounds. One male model had a long snood and many side caruncles 
(highly ornamented) and the other had a shorter snood and fewer side caruncles (slightly 
ornamented). The models were placed 1.3 m apart at one end of the rectangular arena 
(Figure 4-lb). The relative positions of the highly ornamented and slightly ornamented 
models were randomized. Approximately 15 ml of bird seed was placed in a pile on the 
ground immediately below the bill of each model. Males were denied food for a few hours 
immediately before the trial, but this appeared to have little impact on their behavior because 



57 

they did not feed immediately when food was returned after the trial. In any case bird seed 
was a preferred treat that the turkeys would eat preferentially even when their regular food 
was available ai libitum . During each model trial a single male was admitted through a door 
in one side of the arena. The latency of the males to feed from one of the seed piles was 
recorded. Males that did not choose a seed pile within 30 min were removed and were not 
retested. 

Results 

Live Male Trials 

Fighting occurred in 8 of the 14 trials. Fights lasted on average only 46.1 sec. Out 
of the 6 trials in which no fighting occurred, there were three cases in which the subordinate 
male fled from the other male immediately. In one case the males did not fight nor flee, nor 
did they ever direcdy contact one another. The duration of fighting showed a trend toward 
being negatively correlated with differences in beard length between the two males (r s = 
-0.51, p=0.07). During fighting only 2 of the 28 males tested, distended their snoods 
slightly (just past the bill opening). In both cases these males were later classified as 
dominant to the individual with which they were paired. 

Seven of the ten male characteristics measured directly were found to be strongly 
correlated (r 2 >0.4) with one another (Table 4-1). These were spur length, relaxed snood 
length, side caruncle number, skullcap width, frontal caruncle area, frontal caruncle depth 
and body mass. A factor analysis utilizing varimax transformation produced four factors 
from these variables (Table 4-2). Snood length and mass loaded on the first factor, spur 
length, frontal caruncle area and caruncle depth loaded on the second factor, skullcap width 
loaded on the third factor and side caruncle number loaded on the fourth factor. The factor 
scores of these variables are analyzed below in addition to the raw measurements in an 
attempt to identify underlying axes of variation in these characters. 



58 



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The differences between the two males scores on factors 2, 3 and 4 were not 
significantly different from zero (mean differences = -0.14, 0.5, 0.11, respectively; Table 4- 
3). However the results for factor 1, though only nearly significant, suggest that snood 
length and body mass may be associated with dominance in male wild turkeys (mean 
difference = 0.48). When the difference between dominant and subordinate males in these 
characters are assessed direcdy, without the aid of factor analysis, relaxed snood length is 
the only character that is significantly different between the two groups (Table 4-3). 
However dominant males on average had higher values for all ten of the variables measured 
(Binomial test, N=10, one-tailed, P=0.06). 

Individuals that started fights were no more likely to become dominant than those 
that responded to the threat behavior (X 2 =2.27, v=l, p> 0.05). The time until first contact in 
the 13 trials in which contact occurred averaged 129.2 sec, although 85% were 32 sec or 
less. The difference in ornamentation of the males was associated with the time until first 
contact between males that actually fought The time until first contact was positively 
correlated with differences between males on the second factor (spur length, caruncle area 
and depth; r s = 0.52, n=13, p=0.07). This relationship was statistically significant if the raw 
differences in spur length are tested rather than the factor scores (r s = 0.59, p=0.04). The 
difference in the frequency of wingflapping bouts prior to contact, on the other hand, was 
negatively associated with time until first contact, although only nearly significantly (r s = 

-0.50, p=0.08). 

The males had been divided into two matched groups for the dominance trials: 
nondisplayers and displayers. The eleven displayer males tended to have longer stretched 
snoods (4.0 vs. 4.6 cm; U=56, U!=131, p=0.08) and larger factor two scores (spur, frontal 
caruncle area and depth; U=52, U ! = 135, p=0.05). However only caruncle depth was 
significantly different when the raw values of these variables were compared between the 
two groups (1.0 vs 1.2 cm; U=30.5, U l = 156.5, p=0.003). 



61 



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Male Model Trials 

Twenty one of the 28 males tested responded by feeding within the 30 min trial 
period. Of the seven males that did not respond, two attacked the decoys (one gave fighting 
purrs to the less ornamented model, the other pecked the snood of the more ornamented 
model), four did not feed or approach the decoys, and one trial was excluded because a 
decoy toppled over. A significant number of the 21 males that responded under the trial 
conditions fed in front of the less ornamented decoy (X 2 = 8.0, v=l, p< 0.01). The four 
males who chose to feed from the seed in front of the more ornamented male tended to have 
smaller spurs (mean= 2.1 vs. 1.3 cm; U= 22.5, U*= 73.5, p=0.09) and fewer side caruncles 
(25.7 vs. 12.8; U=18, U 1 =78, p=0.05) than the 17 who fed in front of the less ornamented 
model. The latency of the males to feed (i.e. the time from the start of the trial until males 
began to feed) was not correlated with any of the male characters measured. The males who 
did not feed during the trial were not different from the other males in any of the measured 
characters (Mann Whitney U-tests, all p> 0.05). 

Discussion 

In dyadic encounters between wild turkeys the only male character significantly 
predictive of the outcome of male-male interaction was relaxed snood length. Dominant 
males had longer relaxed snoods than their subordinate partners. Similarly males tended to 
avoid feeding on seeds near model males with longer snoods in the male model trials. 
These complementary results strongly suggest that males assess one another's snood length 
as an indicator of male condition and status. Therefore it is surprising that differences in 
snood length do not affect the time until, or duration of, combat If snood length is a good 
indicator of status, males with similar snood lengths should need to battle longer to resolve 
relative dominance status than pairs of males with very disparate snood lengths. Additional 
studies are necessary to understand why males do not adjust their investment in fighting 
according to their likelihood of winning. 



63 

Differences in several other male characters showed tendencies to be correlated with 
the time until first contact and the duration of fighting. Males with similar spur lengths 
fought each other sooner after meeting than dissimilar males. Spurs serve as weapons 
during battle in a number of galliforms (Davison 1985) including wild turkeys, but none of 
the evidence shows that the length of spurs affects the outcome of combat. In fact an 
experimental field study in Sweden clearly demonstrated that variation in the length of spurs 
is not a good predictor of dominance status in ringneck pheasants (Phasianus colchicus ). 
although this character is assessed by females during mate choice (von Schantz et al. 1989). 
Spur length in wild turkeys is a reliable predictor of age (Kelly 1975) and older males tend 
to be larger and in better condition (Chapter 3). Therefore spur length may normally be 
assessed by competitors before battle in the wild where different aged animals encounter 
one another, but is of little significance in the outcome of trials where males are of the same 
age as was the case here. 

Differences in the frequency of wingflapping bouts, a behavior associated with 
aggressiveness in other galliforms, tended to be negatively correlated with time until first 
contact However this behavior did not occur at a higher frequency in dominant individuals. 
Similarly differences in beard length between males tended towards a negative correlation 
with duration of fighting. The greater the difference in beard lengths between males the 
more quickly they tended to resolve fights. However beard length was not a good predictor 
of dominance status either. Beard length increases with age to some degree (Kelly 1975), 
but is strongly affected by abrasion and thus is probably not a consistent indicator of age 
across different habitats (Pelham & Dickson 1992). Studies of beard and spur 
development relative to agonistic interactions in mixed-age populations are needed. 

In captivity males classified as "displayers" had longer stretched snoods than 
nondisplayers. I did not test the relative dominance of these two types of males. Off hand 
it might seem reasonable to conclude that displayers will be dominant over nondisplayers 
because displayers have longer stretched snoods. However more caution in interpreting the 



64 

implications of stretched snood lengths is necessary. Snood distension is muscular (Lucas 
& Stettenheim 1972), therefore the difference in stretched snood length between displayers 
and nondisplayers may possibly be attributable to the greater exercise given the snood by 
the "displayer" males. Additional evidence to support this hypothesis comes from the 
previous chapter (Chapter 3) where average display rate (a measure of how often the snood 
is distended) was found to be strongly correlated with stretched snood length but only 
weakly correlated with relaxed snood length. For this reason it is unclear whether 
displaying males can be assumed to be dominant over nondisplayers based on 
ornamentation differences. This cautionary note serves as a reminder that behavior can 
influence morphology just as the reverse is true. 

Snood length was strongly correlated with body mass, a factor thought to be very 
important to resource holding capacity and the outcome of dyadic encounters in many 
species (Parker 1974; Richner 1989; Beaugrand et al. 1991). In this study males differed 
by several kilograms in weight in some cases, and yet this variable, when measured alone, 
did not have a significant effect on the outcome of fighting. Snood length, on the other 
hand, was greater in dominant males when raw measurements were used and nearly so when 
factor scores were used. This suggests that snood length indicates more than just body 
mass to potential competitors. Results presented earlier (Chapter 3) confirm that snoods are 
good indicators of a number of measures of male condition, including parasite burden, 
energy reserves and possibly age. My results suggest that males use snood length as a 
general measure of the risks associated with fighting over food or status and that females 
use this male character to assess male condition and fighting success. 

Similar results were obtained in comprehensive studies of sexual selection in red 
junglefowl, Gallus gaUus : (Ligon et al. 1990; Zuk et al. 1990a; 1990b; 1992). Comb length 
in this species is maintained by female choice. Females choose males based on comb 
length because this character indicates male parasite burden and fighting success. Thus the 
comb of junglefowl and the snood of wild turkeys fit Borgia's (1979) War Propaganda 



65 

model for the evolution of extravagant ornamentation because females are choosing males 
based on characters that indicate male fighting success. 

In contrast studies of sexual behavior and fleshy ornamentation in grouse suggest a 
different scenario than that in phasianids. Comb size is a good indicator of male status in 
ptarmigans (Gjesdal 1977; Moss et al. 1979; Stokkan 1979) and affects how males interact 
(Holder & Montgomerie 1993), but this character is not under direct selection by females. 
Instead female ptarmigan preferentially mate with males whose combs show less damage 
from fighting. In larger grouse comb characteristics appear to be unimportant to female 
mate choice (Alatalo et al. 1991). Why do females assess male fleshy ornamentation 
differently in phasianids and grouse? One reason may be that phasianids have permanently 
exposed fleshy ornaments, while grouse can hide their combs beneath feathers. The 
facultative nature of comb exposure makes it more difficult for females to assess the size of 
the comb. As a consequence females are selected to base their mate choice on a more easily 
and quickly assessed characteristic (Sullivan 1994), such as scarring and damage from 
fighting (Brodsky 1988). This interpretation is at best speculative but warrants further 
investigation. 

In conclusion it appears that female and male wild turkeys can use male fleshy 
ornamentation to assess male condition and dominance status. Male characteristics that are 
important in other species, such as body mass or age, were not valid predictors of the 
outcome of male-male agonistic interactions in this study or were not included as a variable. 
Fleshy ornamentation appears to be an indicator of male status because it is probably 
dependent on a condition- and dominance-dependent hormone, testosterone. Both males 
and females seem to take advantage of the information provided by snood length to increase 
their fitness. 



CHAPTER 5 

THE THERMOREGULATORY ROLE OF THE 

UNFEATHERED HEAD AND NECK IN MALE WILD TURKEYS 



Introduction 

Endotherms usually maintain body temperatures above environmental temperature at 
considerable energetic cost An unexplained exception to the general endotherm pattern of 
having insulation against heat loss are birds that have brightly colored areas of unfeathered 
skin on their heads and necks. Although the bright coloration of these structures is 
consistent with a sexually selected function, some studies have suggested that these areas of 
bare skin also maintain sublethal brain temperatures by dissipating heat via cephalo-cervical 
retes (Crowe & Crowe 1979; Crowe & Withers 1979; LaRochelle et al. 1982; Chapter 2). 
The heat dissipation hypothesis is supported by correlative studies showing that unfeathered 
head and neck skin is maximally exposed at high temperatures and that in some taxa the 
size of unfeathered areas is greater at low latitudes where heat dissipation may be of greater 
importance (Crowe 1979; Chapter 2). Highly vascularized fleshy ornamentation presents a 
functional puzzle when species are distributed over a large latitudinal range in which they 
are exposed to both temperature extremes. Although these species may benefit by using 
their FS to dissipate heat under hot conditions, the uninsulated nature of these structures 
subjects them to extreme heat loss under cold conditions and heat gain in the presence of 
solar radiation. In this study I test the possible thermoregulatory function of unfeathered 
head ornamentation in a species that commonly faces extremes of cold and heat, the wild 
turkey (Meleagris gallopavo) . 

Wild turkeys occur over a broad range of temperature extremes from their southern 
limit in southern Mexico to their northern limits along the US-Canada border (Dickson 



66 



67 

1992). Males are twice as large as females, and have brightly colored unfeathered skin on 
their heads and necks. In addition this skin is covered with polyp-like elaborations of the 
integument called caruncles. A thin dewlap extends from the mandible down to the neck. 
Perhaps most distinctive is the bare, distensible frontal process or snood that projects from 
the forehead at the base of the upper bill. 

Fleshy head ornamentation in wild turkeys and other galliformes is often thought to 
be maintained by sexual selection, that is, it functions in mate choice and male-male 
competition. Ample empirical evidence supports this contention (Brodsky 1988; Boyce 
1990; Hillgarth 1990; Ligon et al. 1990; Zuk et al. 1990a; 1990b; Spurrier et al. 1991; Zuk 
et al. 1992; Chapters 3 & 4;). A role in sexual selection, however, does not rule out 
concurrent functions for these structures in thermoregulation. To understand why the 
unfeathered areas of turkeys are maintained despite the possible costs in terms of heat loss, 
the thermoregulatory tradeoffs faced by wild turkeys with feathered and unfeathered heads 
must be assessed. Because all extant wild turkeys have bare heads, in this study I 
experimentally insulate the heads and necks of turkeys, to assess the thermoregulatory 
tradeoffs that ancestral turkeys may have faced at cold and hot temperatures. 

Methods 

Subjects and Apparatuses 

Eight, two-year old, male wild turkeys, obtained as chicks from a game farm (L&L 
Pheasantry, Hegins, PA, USA), were used in the metabolic trials. These birds were reared 
as described in Chapter 3. Gray and Price (1988) showed no difference in the metabolic 
rates of wild turkeys from game farm or free-living sources. Average body weight of these 
individuals was 7.1 kg (range 6.4-8.1 kg). During the study period (June- Sept 1993) the 
birds were provided with feed (Purina Gamebird Maintenance, 12% protein) and water ad. 
libitum . Subjects were denied food for 26-29 hrs immediately prior to each metabolic trial 



68 

to insure that they were post-absorptive. Post-absorptive conditions are necessary to 
measure the basal or minimum rate of metabolism. Water was still available during the pre- 
trial period. 

Oxygen consumption and total water loss were measured in an open system 
(described by McNab 1988). The temperature of the 329 liter metabolic chamber was 
regulated by pumping water from a water bath through the chamber's hollow walls. Room 
air was sucked through the metabolic chamber, pumped into glass columns filled with soda 
lime (to remove CO2) and silica gel (to remove H2O), after which flow rates, which averaged 
20.6 1/min, were measured by a Brooks Sho-Rate flowmeter. Subsequently the airstream 
was sampled with an Applied Electrochemistry S-3A oxygen analyzer. The temperature 
and humidity of room air varied very little, 23.5 °C (±0.0) and 61.2% (±0.2), respectively. 
Humidity in the chamber was not controlled. The bird's evaporative water loss was 
measured gravimetrically, that is, by weighing the silica gel. Core body temperature was 
measured by inserting a copper-constantan thermocouple, tipped with a thin layer of 
silicone, into the cloaca of the bird to a depth of 20 cm. This measurement was taken 
immediately before the subject was placed in the metabolic chamber and immediately after it 
was removed from the chamber. Six surface temperature measurements were taken: feather, 
leg, body skin, head skin, frontal caruncle and dewlap. Surface temperatures were measured 
with a bare-tipped thermocouple held against the appropriate spot while the subject was still 
in its holding box before the trial and again while it was still in the metabolic chamber at the 
end of a trial. Skin and feather surface temperature were measured approximately 3 cm 
ventral to the carpal joint of the wing. Leg temperature was measured immediately posterior 
to the third scale below the tarsal joint on the left or right leg, depending on which was 
accessible. Head skin temperature was measured on the back of the head at a point in line 
with the lower mandible. Surface temperature of the frontal caruncles and dewlap were 
measured at their approximate centers. 



69 

Different rates of physical activity across subjects and trials can make it difficult to 
detect the effect of experimental treatments on metabolic rate. Therefore I minimized the 
bird's activity by conducting trials at night in the dark. Metabolic trials lasting 2.5 hours 
were conducted between 20:00-03:00 hours. All subjects were given at least one day 
between trials. Individual turkeys were tested at the same time of day (either 20:00 or 0:00 
hours) across all treatments to minimize circadian effects on matched comparisons of 
metabolic rate. The first 30 min of each trial served as an equilibration period during which 
the bird calmed down after handling. The least observed rate of oxygen consumption 
(corrected to standard pressure and temperature) measured during each of the four 
subsequent 30 min periods was used to calculate an average metabolic rate for the entire 
trial. All individuals were given two 2.5 hr habituation trials prior to the experimental trials. 
Usually the subjects rested quietly during the experimental trials. Behaviorial states were 
recorded by instaneous sampling (Martin & Bateson 1986) every 30 min. Three states 
were noted as present or absent: standing, head tucked under feathers, panting. 
Observations were made with the aid of a flashlight through a small window in the chamber. 

Experimental Design 

To determine the potential thermoregulatory impact that head feathering would have 
on wild turkeys, their thermal balance was ascertained when their heads were "bare" (see 
below) and when they were insulated as though they were feathered. To approximate the 
insulatory properties of head and neck feathering, the bare head and neck of the turkey 
were covered with a double layer (0.6 cm on head, 0.9 cm on neck) of acrylic sock (Adler® 
"Casual Acrylic Crew," 75% Hi-Bulk Acrylic/25% Stretch Nylon) with large holes for the 
eyes and the entire bill. Any irritational effects of the insulatory head covering on metabolic 
rate were controlled by placing a hood made of thin, nylon netting with little insulatory value 
on the heads of the "bare" individuals. The control head net and insulatory head socking 
were held in place with small alligator clips that attached to the back and chest feathers at the 



70 

base of the neck. The efficacy of using head socking to approximate the insulation 
provided by normal feathering was determined by studying the warming curves of the 
feathered and unfeathered/reinsulated heads of domestic roosters (Gallus gallus) . 

Six dependent thermoregulatory variables may be affected by head insulation. 
Metabolic rate, as measured by oxygen consumption (cm 3 02/g*hr), is a measure of the 
work the animal does to maintain thermeostasis. Rate of evaporative water loss (g/hr) is a 
measure of the heat lost via evaporation. Metabolic heat production (Hm) and evaporative 
heat loss (H e ) can be converted to common units (mW/g) to compare the cooling capacity 
of the animal in different treatments. Cooling capacity is the ability of the animal to 
dissipate metabolically produced heat by evaporation. It is expressed as a percentage, 
calculated as the heat lost by evaporation divided by the heat produced by metabolism 
(100% x He/H m ; Calder & King 1974). Total thermal conductance (mW/cm 2 °C) 
measures all the heat lost by the animal, including evaporative heat loss, and is the inverse of 
insulation. It is estimated using the values for heat production, and ambient and body 
temperatures. Dry thermal conductance on the other hand is a measure of all 
nonevaporative means of heat loss: radiation, convection and conduction. If total 
conductance is exceeded by heat production, heat is stored in the tissues of the animal and 
body temperature rises. Each of these variables may be varied by the animal to cope with 
increased head and neck insulation. 

Thermoregulatory trials were conducted twice for each turkey at each of three 
ambient temperatures (0, 22, 35 °C); one time as a control, the other with its head insulated. 
These temperatures were chosen to be below, within and above, respectively, the zone of 
thermal neutrality (Gray & Price 1988). The temperatures are also within the range that 
turkeys experience in the wild. A total of 48 trials were conducted. This matched design 
compares the metabolic values of each turkey in the experimental treatment to the values 
obtained from the same bird in the control treatment. This serves to minimize the effects of 
inter-individual variation on the effect of the experimental treatment. Due to scheduling 



71 

conflicts in the laboratory, every turkey was tested at °C before it was exposed to the other 
temperatures. The presentation order of the trials at 22 and 35 °C was randomized. 
Repeated measures ANOVAs were used to test the effects of body size (mean = 6.7 vs. 7.5 
kg for small and large, respectively), chamber temperature and head insulation on oxygen 
consumption (cm 3 02/g*hr), cooling capacity, total and dry thermal conductances (mW/cm 2 
°C) and changes in body and surface temperatures (°C). The effect of each 30 min 
sampling period was also included when oxygen consumption was the dependent variable. 
Treatment groups exhibited similar variances (Fmax tests, all p>0.05; Sokal & Rohlf 1981). 
Reported p values have been adjusted using Greenhouse-Geisser epsilon values. This 
technique conservatively compensates for the use of repeated measures by adjusting the 
degrees of freedom (Abacus Concepts Inc. 1989). 



Results 



The mass specific rate of oxygen consumption was significantly lower for large 
individuals across all temperatures (mean= 0.4140 ±0.007 vs. 0.4730 ±0.013 cm 3 02/g*hr; 
Table 5-1). Rate of metabolism was not significantly different for uninsulated and insulated 
turkeys at and 22 °C. However at 35 °C insulated turkeys exhibited a significantly higher 
average metabolic rate than uninsulated turkeys (Table 5-2, Figure 5-1). A significant, 
three-way interaction between head insulation, temperature and time period suggests that the 
effects of head insulation became more pronounced the longer the subject was exposed to 
the chamber conditions at hot temperatures. 

When the cooling capacities of uninsulated and insulated turkeys were compared, 
uninsulated turkeys demonstrate a significantly greater ability than insulated turkeys to 
dissipate excess metabolic heat by evaporation at 35 °C, but not at cooler temperatures 
(Figure 5-2). Total thermal conductance increased with temperature. It was also greater for 
insulated birds overall (Table 5-1, Figure 5-3) but this difference was significant only at the 



72 

hottest temperature (Table 5-2). Dry thermal conductance decreased with increasing 
temperature in the uninsulated birds. Insulated birds showed a similar pattern of 
conductances at and 22 °C but had significantly higher values than uninsulated birds at 35 
°C. 

Head insulation resulted in significantly greater core body temperature changes of 
birds at 35 °C, but not at the lower temperatures tested (Figure 5-4). Head insulation served 
to keep head skin warmer at °C (31.2 ±1.0 °C uninsulated vs. 36.7 ±0.3 °C insulated), 
but did not result in significantly higher skin temperatures at 22 and 35 °C. Insulated 
turkeys at 22 °C increased their dewlap temperatures significantly more than uninsulated 
birds (32. 1 ±0.7 °C uninsulated vs 35.2 ± 0.3 °C insulated), but this was not true at or 
35 °C. Body skin, feather, frontal caruncle and leg temperatures all increased with 
increasing ambient temperatures, but were not affected by the insulation treatment (Table 5- 

1). 

Across and within each temperature treatment, head insulation had no effect on the 
proportion of instantaneous observations in which the subjects were seen to be standing, 
panting, or had their head tucked in back feathers or under the wing (Mann-Whitney U 
tests, N=16, all p»0.05). Panting only occurred at 35 °C. The frequency of panting was 
difficult to observe because the birds often held their necks forward and down so that the 
view from the small window was blocked by the bird's body. Therefore it is not possible to 
look for associations between panting frequency and thermal balance. Nevertheless upon 
opening the chamber at the end of the 35 °C trials, panting and an elongated snood (only 
visible in uninsulated trials) were observed in all individuals. Snood elongation did not 
occur at other temperatures. 

Although the proportion of observations in which the subjects were standing was 
not influenced by the insulation treatment, the frequency of this behavior did influence some 
of the dependent thermal variables. Frequency of standing was significantly 



73 



Table 5-1. Partial results of repeated measures ANOVAs showing statistically significant 
sources of variation in, and those with strong trends of influence on, the dependent 
measures of thermal balance listed. 



Dependent Variable 


Source of Variance 


df 


F value 


Probab 


Oxygen 
Consumption 


Size 

Insulation*Temp 

Insul*Temp*Time 


1 
2 
4 


5.96 
4.16 
4.15 


0.050 
0.053 
0.043 


Cooling Capacity 


Temperature 
Insulation*Temp 


2 
2 


135.00 
8.87 


0.0001 
0.014 


Thermal 
Conductance (Total) 

Thermal 
Conductance (Dry) 


Insulation 

Temperature 

Insulation*Temp 

Insulation 

Temperature 

Insulation*Temp 


1 
2 
2 

1 

2 
2 


7.19 

367.00 

8.03 

5.30 
9.45 
7.96 


0.037 

0.0001 

0.028 

0.061 
0.016 
0.027 


Core Body 
Temperature 


Insulation 

Temperature 

Insulation*Temp 


1 
2 

2 


6.62 
22.10 
10.39 


0.042 
0.002 
0.011 


Leg Temperature 


Temperature 


2 


150.00 


0.0001 


Skin Temperature 


Temperature 


2 


3.70 


0.086 


Feather Temperature 


Insulation 
Temperature 


1 
2 


4.43 
42.01 


0.083 
0.001 


Head Skin 
Temperature 


Insulation 
Temperature 


1 
2 


12.09 
16.28 


0.013 
0.001 


Frontal Caruncle 
Temperature 


Temperature 


2 


6.39 


0.013 


Dewlap Temperature 


Temperature 
Insul*Temperature 


2 

2 


6.83 
7.79 


0.014 
0.009 



74 



Table 5-2. Mean values of dependent thermal variables in eight wild turkeys exposed to 
three ambient temperatures (°C) with their bare heads and necks uinsulated or insulated. 
Values presented for temperature measurements are mean changes in temperature (end of 
trial value minus beginning of trial value). 



Dependent Variables 


Means 

(±SE) 

UNINSULATED HEADS 


Means 

(±SE) 

INSULATED HEADS 




0» 


22« 


35° 


0° 


220 


35° 


Oxygen Consumption 


0.45C 
(0.02) 


0.41 
(0.01) 


0.43 a 
(0.02) 


0.48C 
(0-24) 


0.40 
(0.01) 


0.50 a 
(0.02) 


Cooling Capacity 


24.68 
(3.31) 


76.83 
(5.47) 


119.69 a 

(7.33) 


29.51 
(3.27) 


84.90 
(3.33) 


96.73 a 

(4.32) 


Thermal Conductance (Total) 


0.11 
(0.01) 


0.24 
(0.01) 


0.78 a 
(0.03) 


0.12 
(0.01) 


0.23 
(0.01) 


0.92 a 
(0.06) 


Thermal Conductance (Dry) 


0.09 
(0.10) 


0.06 
(0.02) 


-0.15 a 
(0.05) 


0.09 
(0.12) 


0.04 
(0.01) 


0.44 a 
(0.05) 


Core Body Temperature 


-0.44 
(0.17) 


-0.44 
(0.12) 


0.36 a 
(0.13) 


-0.35 
(0.15) 


-0.45 
(0.11) 


1.49 a 
(0.37) 


Leg Temperature 


-16.96 
(1.53) 


0.00 
(0.62) 


2.54 
(0.48) 


-19.15 
(3.10) 


-0.11 
(0.69) 


3.31 
(0.64) 


Skin Temperature 


-2.39 
(1.80) 


-1.21 
(1.86) 


2.61 
(1.34) 


-2.71 
(2.43) 


-0.16 
(1.21) 


2.48 
(0.68) 


Feather Temperature 


-8.99 
(1.67) 


1.15 
(0.39) 


5.45 
(0.73) 


-11.01 
(1.49) 


0.73 
(0.63) 


3.86 
(1.54) 


Head Skin Temperature 


-3.03 b 
(1-37) 


-0.16 
(0.45) 


2.30 
(0.73) 


0.7 l b 
(0.33) 


1.11 
(0.43) 


2.96 
(0.42) 


Frontal Caruncle 
Temperature 


-1.98 
(1.05) 


-0.71 
(0.70) 


1.46 
(0.63) 


-5.48 
(4.56) 


1.59 
(0.80) 


3.94 
(0.82) 


Dewlap Temperature 


-0.20 
(0.77) 


-1.94 a 
(1.06) 


2.89 
(0.78) 


-0.87 
(0.56) 


2.53 a 
(0.52) 


2.70 
(1.18) 



Statistically significant differences between values of uninsulated and insulated birds at the 
same temperature have the following probabilities: a <0.01; b <0.05; 0.09> c >0.05. 



75 



OC 



22 C 



35 C 



* 

6>0 



o 

d 
I 



I 

£3 
U 

>•» 

O 



0.8 



0.6- 



0.2 



■ 

D 

■ 

■ 
D 


n ■ _n 
■ ■d ■■ 


■ D 

D ■ 

m 

■ D 



Individual Turkeys 



Figure 5-1 . Oxygen consumption of eight turkeys with heads 
uninsulated (empty squares) and insulated (filled squares) at three ambient 
temperatures. Presented in order of increasing body mass. 



76 



OC 



22 C 



35 C 



# 



8 

o 

(SO 

a 

Q 

O 

O 



zuu- 








150- 






D D 








DD 


100- 




■ 

D "■ 

□ 


■3 - iD D 

■ ■ , 


50- 


■ o 


D 


■ 


■ 


° "5-5- 

n no ■ 






0- 


■ 







Individual Turkeys 



Figure 5-2. Cooling capacities of eight turkeys with heads uninsulated 
(empty squares) and insulated (rilled squares) at three ambient 
temperatures. Presented in order of increasing body mass. 



77 



OC 



22 C 



35 C 



U 



! 

8 



o 
a 

-a 

a 

o 

u 



o 



l.f 








1.2- 






■ 


1.0- 






■ ■ ' 


0.8- 






■ i 


0.6- 






a 


0.4- 






• 


0.2- 

a . 


E 
■ ■■Hlflfl 


gi|E |H H H 


< 



Individual Turkeys 



Figure 5-3. Total thermal conductances of eight turkeys with heads 
uninsulated (empty squares) and insulated (filled squares) at three ambient 
temperatures. Presented in order of increasing body mass. 



78 



U 



oc 



22 C 



35 C 



I I M^— ■— 



«■—•—■_ 



I 1 



T3 

O 

PQ 
§ 

5 



1> 
so 



6 



2 



o- 



■H 



iB 
n 



D 



» ■ -^^^^^^^^^^^^^ 



Individual Turkeys 



Figure 5-4. Change in core body temperature of eight turkeys with heads 
uninsulated (empty squares) and insulated (filled squares) at three ambient 
temperatures. Presented in order of increasing body mass. 



79 

correlated with higher head skin temperatures at °C (both insulation treatments combined, 
r s = 0.54, p=0.05) and is associated with a tendency for lower rates of metabolic heat 
production (r s = -0.50, p=0.07). At 22 and 35 °C, feather temperature inversely correlated 
with standing frequency (r s = -0.66, p=0.01 and r s = -0.52, p= 0.05, respectively). 

Head tucking occurred in eight of 16 trials by six different individuals at °C. 
Higher frequencies of head tucking were positively, though only nearly significantly, 
correlated with changes in feather and dewlap temperatures (r s = 0.49, p=0.08 and r s = 0.50, 
p=0.05, respectively), and negatively correlated with changes in skin temperature (rho= 
-0.58, p=0.04), changes in core body temperature (r s = -0.54, p= 0.05), metabolic heat 
production (r s = -0.56, p= 0.05) and both total and dry conductance (r s = -0.56, p= 0.05 and 
r s = -0.66, p= 0.02, respectively). 

Discussion 

A dramatic cost of insulated heads and necks occurs in male wild turkeys at high 
temperatures. Insulated males had higher metabolic rates and markedly increased core body 
temperatures. Associated with this were increased dry and evaporative thermal 
conductances over uninsulated males at the same temperature. However the much lower 
cooling capacities of insulated males reveals their relative inability to dissipate metabolic 
heat by evaporative heat loss. These results demonstrate that the unfeathered heads and 
necks of male wild turkeys, and possibly the fleshy structures on the head, contribute to heat 
dissipation at high ambient temperatures. 

Contrary to expectations, under cold conditions head and neck insulation did not 
significantly reduce thermal conductance or increase metabolic heat production. Under cold 
conditions free living wild turkeys often contract the skin at the back of their necks, 
effectively drawing the feathered skin at the base of the neck up and over much of the 
usually bare areas of the back of the neck (personal observation). The captive wild turkeys 
in this study exhibited similar behavior, possibly explaining the absence of a difference in 



80 



thermal conductance between uninsulated and insulated birds at °C. Because winter 
starvation can be an important source of mortality for turkey populations in the northern 
part of their distribution (Healy 1992b), reducing heat loss from the head may enhance 
turkey survivorship. At night thermal conductance may be further decreased by tucking the 
head under the wing or back feathers. In this study four of the eight uninsulated individuals 
at °C were seen to have their heads tucked during at least one of the observation periods. 
Three of these had lower metabolic rates than the remaining individuals, providing support 
for this explanation. LaRochelle et al. (1982) found a similar effect of head tucking in black 
vultures, which also have unfeathered heads. Additional studies of the effect of artificial and 
behavioral head insulation on heat production and loss in wild turkeys are needed at low 
temperatures. 

Other birds have modified unfeathered areas to control heat loss. Ptarmigan 
(Lagopus spp.), which live at high latitudes and altitudes where the difference between body 
temperature and ambient temperature can be large (e.g., > 60 °C), often have legs and feet 
that are feathered (Johnsgard 1983). Other species limit heat loss in cold conditions with 
vascular modifications. Gulls (Laridae) have counter-current heat exchange mechanisms 
that reduce heat loss from the feet under cold conditions (Baudinette et al. 1976). The wood 
stork (Mycteria americana) and turkey vulture (Cathartes aura ) use their unfeathered legs to 
dump heat at hot temperatures and are able to enhance this mechanism of heat loss by 
defecating on their legs to promote evaporative heat loss (Kahl 1963; Hatch 1970). Ducks 
may utilize the large surface area of their bills to dissipate heat (Hagan & Heath 1980). The 
wild turkeys used in this study are the only species in which the value of unfeathered heads 
and necks for heat dissipation has been demonstrated experimentally. 

Previous studies of the metabolism of the wild turkey have ignored the metabolism 
of wild turkeys at temperatures above 25 °C (Gray & Price 1988; Oberlag et al. 1990). The 
adaptive benefit of unfeathered heads demonstrated here suggests that peak effective 
temperatures during the reproductive season, especially in habitats without shade, may limit 



81 

wild turkey distribution or population density. These results are reinforced by early studies 
on the temperature requirements of domestic turkeys. High ambient temperature 
(approximately 30 °C) and exposure to direct sunlight may reduce male fertility by as much 
as 10% in Broad-Breasted Bronze turkeys, the domestic breed most similar in appearance to 
wild turkeys (Kosin & Mitchell 1955). Wilson and Woodard (1955) found that all 
domestic turkeys were subject to hyperthermia at ambient temperatures above 32 °C, but 
that this was particularly true of large males. In addition body temperature and water 
consumption by domestic turkeys were inversely correlated with the percent shade cover 
provided at ambient temperatures above 35 °C (Wilson et al. 1955; Wilson & Woodard 
1955). Wild turkeys experienced heat stress at 35 °C in the lab in this study. All males 
responded to hot chamber temperatures by panting, dropping their wings, and extending 
their necks and snoods. One individual (no. 1) even became frantic at the very end of both 
high temperature trials and was removed immediately. Behavioral changes that occur in 
free-living wild males under hot conditions provide similar support. 

Mature male turkeys in northern Florida seem to avoid bright sun and in the 
summer are found standing in heavy shade with dewlap and neck bright red and extended 
while panting heavily (personal observation). Also it seems that males are more reluctant to 
flee under these conditions and can be approached more closely than when it is cooler. 
Males are faced with a thermoregulatory quandry under hot, sunny conditions. Resting 
quietly in the shade maintains sublethal body temperatures but does not allow feeding, 
fighting for access to mates, or displaying to females. These latter activities, however, are 
also functionally and adaptively necessary, but result in metabolic heat production and 
exposure to solar radiation. Field studies of the behavior of wild turkeys relative to 
environmental conditions, including radiative heat load and wind speed, are needed to 
understand how males tradeoff thermal needs with feeding and mating success. The results 
of this study suggest that the bare head and neck of male wild turkeys enables wild turkeys 
to manage these conflicting goals more successfully. 



CHAPTER 6 
GENERAL DISCUSSION 



The unfeathered, ornamented head of male wild turkeys has dual adaptive functions: 
it indirectly increases mating success and directly increases heat dissipation at high 
temperatures. The FS of wild turkeys increases mating success in two ways. Male snood 
length, is strongly correlated with both female choice and male dominance. A negative 
correlation between snood length and number of coccidia oocysts found in the feces 
suggests that females use male snood length to detect which males are resistant to this 
debilitating parasite. Females that mate with parasite-resistant males may have increased 
fitness if the male's parasite resistance is heritable, because her offspring will be better able 
to withstand the deleterious effects of parasitism. Longer snooded males were dominant 
over shorter snooded ones and all males avoided interaction with longer snooded artificial 
males. Males may avoid fighting with longer snooded males because of the risks of 
combatting males that are likely to be in better overall condition. 

In addition to these sexually selected functions for some aspects of the unfeathered 
head of wild turkeys, FS are used in thermoregulation. Turkeys whose head and 
ornamentation had been insulated as though covered with feathers were unable to dissipate 
heat at high temperatures. Although the thermoregulatory function of the uninsulated head 
was not experimentally attributed to any one part of the male's head ornamentation in this 
study, the distention of snoods by males at high temperatures suggest that this character 
may be used to dissipate heat. 

The mystery of FS maintenance and evolution in wild turkeys and other galliforms 
was not fully explained by the study of sexual selection and thermoregulation described 
above. The head ornamentation of wild turkeys has several components, only one of which, 

82 



83 

the snood, seemed to be under directional sexual and natural selection. In particular the 
functions of the distinctive side and front caruncles remain unexplained. These characters 
showed considerable variation that could be used by females and other males to discriminate 
among males. Why are these characters maintained? Multiple year, mate choice studies 
have shown that the characters that females seem to be assessing can vary somewhat from 
year to year. It is possible that mate choice may still be an important explanation for these 
characters. Additional studies are needed to address variation in character assessment over 
the lifetime of both males and females in this species. 

Side and frontal caruncles are highly vascularized structures that typically turn 
bright red during display due to increased blood flow. My experimental treatment did not 
selectively insulate these structures, but the increased surface area provided by these 
characters could serve to increase the dissipation of excess body heat over that dissipated by 
the plain bare skin. Thus caruncles may play a role in heat dissipation during male 
courtship display. It may be possible to remove caruncles or restrict blood flow to them to 
study their use in heat dissipation. Experimental studies such as this, coupled with field 
observations of thermoregulatory behavior patterns can clarify the reason fleshy characters 
characters other than the snood are maintained. 

The highly competitive nature of highly polygynous mating systems, such as the 
wild turkey's, is thought to select for increased body size in males. However large body size 
poses a problem for animals in hot climates because their reduced surface area to volume 
ratio makes it more difficult for these species to dissipate heat to the environment As 
described in the second chapter, fleshy structures are larger and more common in larger 
species. This suggests that the need for large fleshy structures in some species is caused by 
increased body size driven by intense sexual selection. Species living in cooler climates and 
small species in any climate should not experience the dilemma posed by hyperthermia, nor 
should species that have low metabolic rates. Studies of fleshy structures relative to body 



84 

size and environmental temperatures in other avian taxa are needed to test the validity of this 
hypothesis. 

Studies of sexual selection rarely consider additional or alternative hypotheses for 
the function of ornamental characters. Sexual selection theory generally assumes that 
greater elaboration of sexually-selected traits carries with it decreased survival. The results 
presented in this dissertation suggest that sexual selection may not necessarily be at odds 
with natural selection. Instead sexual and natural selection may, in some cases, work in 
tandem. The costs of sexually-selected ornaments are assumed to be extreme. However 
attention to non-sexual hypotheses in addition to sexually-selected ones, may reveal that the 
apparent benefits of extravagant characters are multiple and far outweigh the costs. Heated 
debate between theoreticians on the evolutionary stability of different models of female 
choice for male characteristics, has narrowed consideration of other functions for so-called 
ornaments. My work suggests that a general skepticism of the ability of sexual selection to 
explain everything is warranted. "A good field worker is nobody's poodle" (Grafen 1987, 
p.221). 



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BIOGRAPHICAL SKETCH 

Richard Buchholz was born in Manhasset, New York, on 5 November 1964 and 
grew up in nearby Little Neck. His early interest in biology was satisfied by wandering the 
salt marshes and seashore along Little Neck Bay on Long Island Sound and exploring the 
forest during summer trips to his uncle's home in Mountaintop, Pennsylvania. 

He majored in biology at the State University of New York at Binghamton and 
graduated with a Bachelor of Science degree, with outstanding overall performance and 
distinguished independent study in biological sciences, in June 1986. Subsequently he 
studied the reproductive behavior of the yellow-knobbed curassow in the wild in Venezuela 
and in captivity in Mexico for his Master of Science degree, which was granted by the 
University of Florida, Department of Zoology, in August 1989. This work led to his 
interest in the costs and benefits of wattles, ceres and similar structures in birds. He 
received his Doctor of Philosophy degree from the Department of Zoology, University of 
Florida in August 1994. 



94 



I certify that I have read this study and that in my opinion it conforms to acceptable 
l„Jl%i^%**** anally adequate, in scope and quality, as a 
dissertation for the degree of Doctor of Philosophy. 




H: Jane Brockmanrv Chairman 
Professor of Zoology 



I certify that I have read this study and that in my opinion it conforms to acceptable 
stand JSoSly P^entation and i fully adequate, in scope and quahty, as a 
.• ._*:„„ e^iu* Aoarpt* of Doctor of Philosophy. 



stanaaras 01 sunui<ury V i^o^^~~ --., ' . / 

dissertation for the degree of Doctor of Philosophy. 




Richard A. Kiltie 

Associate Professor of Zoology 



I certify that I have read this study and that in my opinion it conforms to acceptable 
sm J^loXv^^iion and is fully adequate, in scope and quahty, as a 
dissertation for the degree of Doctor of Philosophy. 




uougiaj^a. j-^vt-jr / 
Associate Professor of Zoology 



I certify that I have read this study and that in my opinion it conforms to acceptable 
stand Js ^scholarly presentation and is fully adequate, in scope and quality, as a 
dissertation for the degree of Doctor of Philosophy. 



BrianK. McNab 
Professor of Zoology 



I certify that I have read this study and that in my opinion it ™^ to J?fP table 
stand Js of sc'holarly presentation and Lis fully adequate, In scope an^fty, as a 
dissertation for the degree of Doctor of Philosophy. 




Jllis C. Greiner 

Professor of Veterinary Medicine 



sSSaffia^SSSSSSSa 



August, 1994 



7 S&aJI<<iJSm - j&dri 



Dean, Graduate School